The immediate costs and long‐term benefits of assisted gene flow in large populations

With the genetic health of many plant and animal populations deteriorating due to climate change outpacing adaptation, interventions, such as assisted gene flow (AGF), may provide genetic variation necessary for populations to adapt to climate change. We ran genetic simulations to mimic different AG...

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Published inConservation biology Vol. 36; no. 4; pp. e13911 - n/a
Main Authors Grummer, Jared A., Booker, Tom R., Matthey‐Doret, Remi, Nietlisbach, Pirmin, Thomaz, Andréa T., Whitlock, Michael C.
Format Journal Article
LanguageEnglish
Published United States Blackwell Publishing Ltd 01.08.2022
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Abstract With the genetic health of many plant and animal populations deteriorating due to climate change outpacing adaptation, interventions, such as assisted gene flow (AGF), may provide genetic variation necessary for populations to adapt to climate change. We ran genetic simulations to mimic different AGF scenarios in large populations and measured their outcomes on population‐level fitness to determine circumstances in which it is worthwhile to perform AGF. In the absence of inbreeding depression, AGF was beneficial within a few generations only when introduced genotypes had much higher fitness than local individuals and traits affecting fitness were controlled by a few genes of large effect. AGF was harmful over short periods (e.g., first ∼10–20 generations) if there was strong outbreeding depression or introduced deleterious genetic variation. When the adaptive trait was controlled by many loci of small effect, the benefits of AGF took over 10 generations to realize—potentially too long for most climate‐related management scenarios. The genomic integrity of the recipient population typically remained intact following AGF; the amount of genetic material from the donor population usually constituted no more of the recipient population's genome than the fraction of the population introduced. Significant genomic turnover (e.g., >50% replacement) only occurred when the selective advantage of the adaptive trait and translocation fraction were extremely high. Our results will be useful when adaptive management is used to maintain the genetic health and productivity of large populations under climate change. Resumen Con el deterioro de la salud genética de muchas poblaciones de plantas y animales debido a la ventaja que le lleva el cambio climático a la adaptación, algunas intervenciones, como el flujo génico asistido (FGA), pueden proporcionar la variación genética necesaria para que las poblaciones se adapten al cambio climático. Simulamos diferentes escenarios de FGA aplicado en poblaciones grandes y medimos los resultados en la aptitud a nivel poblacional para determinar las circunstancias en las que merece la pena realizar FGA. Cuando no hubo depresión endogámica, el FGA produjo un beneficio en pocas generaciones sólo cuando se introdujeron genotipos que tenían una aptitud mucho mayor que los individuos locales y cuando unos cuantos genes de gran efecto controlaron los rasgos que afectaban a la aptitud. El flujo génico asistido fue dañino en periodos cortos (p.ej.: las primeras 10–20 generaciones) si existía una fuerte depresión exogámica o una variación genética deletérea introducida. Cuando muchos loci de pequeño efecto controlaron el rasgo adaptativo, los beneficios del FGA tardaron más de 10 generaciones en aparecer – un tiempo potencialmente muy largo para la mayoría de la gestión relacionada con el clima. La integridad genómica de la población receptora casi siempre permaneció intacta después del FGA; es decir, la cantidad de material genético de la población donante generalmente no constituyó más que la fracción de población introducida en el genoma de la población receptora. La rotación genómica significativa (p.ej.: reemplazos >50%) sólo ocurrió cuando la ventaja selectiva del rasgo adaptativo y la fracción de reubicación fueron extremadamente elevadas. Nuestros resultados serán útiles cuando se use la gestión adaptativa para mantener la salud genética y la productividad de las poblaciones grandes bajo el cambio climático.
AbstractList With the genetic health of many plant and animal populations deteriorating due to climate change outpacing adaptation, interventions, such as assisted gene flow (AGF), may provide genetic variation necessary for populations to adapt to climate change. We ran genetic simulations to mimic different AGF scenarios in large populations and measured their outcomes on population‐level fitness to determine circumstances in which it is worthwhile to perform AGF. In the absence of inbreeding depression, AGF was beneficial within a few generations only when introduced genotypes had much higher fitness than local individuals and traits affecting fitness were controlled by a few genes of large effect. AGF was harmful over short periods (e.g., first ∼10–20 generations) if there was strong outbreeding depression or introduced deleterious genetic variation. When the adaptive trait was controlled by many loci of small effect, the benefits of AGF took over 10 generations to realize—potentially too long for most climate‐related management scenarios. The genomic integrity of the recipient population typically remained intact following AGF; the amount of genetic material from the donor population usually constituted no more of the recipient population's genome than the fraction of the population introduced. Significant genomic turnover (e.g., >50% replacement) only occurred when the selective advantage of the adaptive trait and translocation fraction were extremely high. Our results will be useful when adaptive management is used to maintain the genetic health and productivity of large populations under climate change.
With the genetic health of many plant and animal populations deteriorating due to climate change outpacing adaptation, interventions, such as assisted gene flow (AGF), may provide genetic variation necessary for populations to adapt to climate change. We ran genetic simulations to mimic different AGF scenarios in large populations and measured their outcomes on population‐level fitness to determine circumstances in which it is worthwhile to perform AGF. In the absence of inbreeding depression, AGF was beneficial within a few generations only when introduced genotypes had much higher fitness than local individuals and traits affecting fitness were controlled by a few genes of large effect. AGF was harmful over short periods (e.g., first ∼10–20 generations) if there was strong outbreeding depression or introduced deleterious genetic variation. When the adaptive trait was controlled by many loci of small effect, the benefits of AGF took over 10 generations to realize—potentially too long for most climate‐related management scenarios. The genomic integrity of the recipient population typically remained intact following AGF; the amount of genetic material from the donor population usually constituted no more of the recipient population's genome than the fraction of the population introduced. Significant genomic turnover (e.g., >50% replacement) only occurred when the selective advantage of the adaptive trait and translocation fraction were extremely high. Our results will be useful when adaptive management is used to maintain the genetic health and productivity of large populations under climate change. Resumen Con el deterioro de la salud genética de muchas poblaciones de plantas y animales debido a la ventaja que le lleva el cambio climático a la adaptación, algunas intervenciones, como el flujo génico asistido (FGA), pueden proporcionar la variación genética necesaria para que las poblaciones se adapten al cambio climático. Simulamos diferentes escenarios de FGA aplicado en poblaciones grandes y medimos los resultados en la aptitud a nivel poblacional para determinar las circunstancias en las que merece la pena realizar FGA. Cuando no hubo depresión endogámica, el FGA produjo un beneficio en pocas generaciones sólo cuando se introdujeron genotipos que tenían una aptitud mucho mayor que los individuos locales y cuando unos cuantos genes de gran efecto controlaron los rasgos que afectaban a la aptitud. El flujo génico asistido fue dañino en periodos cortos (p.ej.: las primeras 10–20 generaciones) si existía una fuerte depresión exogámica o una variación genética deletérea introducida. Cuando muchos loci de pequeño efecto controlaron el rasgo adaptativo, los beneficios del FGA tardaron más de 10 generaciones en aparecer – un tiempo potencialmente muy largo para la mayoría de la gestión relacionada con el clima. La integridad genómica de la población receptora casi siempre permaneció intacta después del FGA; es decir, la cantidad de material genético de la población donante generalmente no constituyó más que la fracción de población introducida en el genoma de la población receptora. La rotación genómica significativa (p.ej.: reemplazos >50%) sólo ocurrió cuando la ventaja selectiva del rasgo adaptativo y la fracción de reubicación fueron extremadamente elevadas. Nuestros resultados serán útiles cuando se use la gestión adaptativa para mantener la salud genética y la productividad de las poblaciones grandes bajo el cambio climático.
With the genetic health of many plant and animal populations deteriorating due to climate change outpacing adaptation, interventions, such as assisted gene flow (AGF), may provide genetic variation necessary for populations to adapt to climate change. We ran genetic simulations to mimic different AGF scenarios in large populations and measured their outcomes on population‐level fitness to determine circumstances in which it is worthwhile to perform AGF. In the absence of inbreeding depression, AGF was beneficial within a few generations only when introduced genotypes had much higher fitness than local individuals and traits affecting fitness were controlled by a few genes of large effect. AGF was harmful over short periods (e.g., first ∼10–20 generations) if there was strong outbreeding depression or introduced deleterious genetic variation. When the adaptive trait was controlled by many loci of small effect, the benefits of AGF took over 10 generations to realize—potentially too long for most climate‐related management scenarios. The genomic integrity of the recipient population typically remained intact following AGF; the amount of genetic material from the donor population usually constituted no more of the recipient population's genome than the fraction of the population introduced. Significant genomic turnover (e.g., >50% replacement) only occurred when the selective advantage of the adaptive trait and translocation fraction were extremely high. Our results will be useful when adaptive management is used to maintain the genetic health and productivity of large populations under climate change. Con el deterioro de la salud genética de muchas poblaciones de plantas y animales debido a la ventaja que le lleva el cambio climático a la adaptación, algunas intervenciones, como el flujo génico asistido (FGA), pueden proporcionar la variación genética necesaria para que las poblaciones se adapten al cambio climático. Simulamos diferentes escenarios de FGA aplicado en poblaciones grandes y medimos los resultados en la aptitud a nivel poblacional para determinar las circunstancias en las que merece la pena realizar FGA. Cuando no hubo depresión endogámica, el FGA produjo un beneficio en pocas generaciones sólo cuando se introdujeron genotipos que tenían una aptitud mucho mayor que los individuos locales y cuando unos cuantos genes de gran efecto controlaron los rasgos que afectaban a la aptitud. El flujo génico asistido fue dañino en periodos cortos (p.ej.: las primeras 10–20 generaciones) si existía una fuerte depresión exogámica o una variación genética deletérea introducida. Cuando muchos loci de pequeño efecto controlaron el rasgo adaptativo, los beneficios del FGA tardaron más de 10 generaciones en aparecer – un tiempo potencialmente muy largo para la mayoría de la gestión relacionada con el clima. La integridad genómica de la población receptora casi siempre permaneció intacta después del FGA; es decir, la cantidad de material genético de la población donante generalmente no constituyó más que la fracción de población introducida en el genoma de la población receptora. La rotación genómica significativa (p.ej.: reemplazos >50%) sólo ocurrió cuando la ventaja selectiva del rasgo adaptativo y la fracción de reubicación fueron extremadamente elevadas. Nuestros resultados serán útiles cuando se use la gestión adaptativa para mantener la salud genética y la productividad de las poblaciones grandes bajo el cambio climático.
With the genetic health of many plant and animal populations deteriorating due to climate change outpacing adaptation, interventions, such as assisted gene flow (AGF), may provide genetic variation necessary for populations to adapt to climate change. We ran genetic simulations to mimic different AGF scenarios in large populations and measured their outcomes on population-level fitness to determine circumstances in which it is worthwhile to perform AGF. In the absence of inbreeding depression, AGF was beneficial within a few generations only when introduced genotypes had much higher fitness than local individuals and traits affecting fitness were controlled by a few genes of large effect. AGF was harmful over short periods (e.g., first ∼10-20 generations) if there was strong outbreeding depression or introduced deleterious genetic variation. When the adaptive trait was controlled by many loci of small effect, the benefits of AGF took over 10 generations to realize-potentially too long for most climate-related management scenarios. The genomic integrity of the recipient population typically remained intact following AGF; the amount of genetic material from the donor population usually constituted no more of the recipient population's genome than the fraction of the population introduced. Significant genomic turnover (e.g., >50% replacement) only occurred when the selective advantage of the adaptive trait and translocation fraction were extremely high. Our results will be useful when adaptive management is used to maintain the genetic health and productivity of large populations under climate change.With the genetic health of many plant and animal populations deteriorating due to climate change outpacing adaptation, interventions, such as assisted gene flow (AGF), may provide genetic variation necessary for populations to adapt to climate change. We ran genetic simulations to mimic different AGF scenarios in large populations and measured their outcomes on population-level fitness to determine circumstances in which it is worthwhile to perform AGF. In the absence of inbreeding depression, AGF was beneficial within a few generations only when introduced genotypes had much higher fitness than local individuals and traits affecting fitness were controlled by a few genes of large effect. AGF was harmful over short periods (e.g., first ∼10-20 generations) if there was strong outbreeding depression or introduced deleterious genetic variation. When the adaptive trait was controlled by many loci of small effect, the benefits of AGF took over 10 generations to realize-potentially too long for most climate-related management scenarios. The genomic integrity of the recipient population typically remained intact following AGF; the amount of genetic material from the donor population usually constituted no more of the recipient population's genome than the fraction of the population introduced. Significant genomic turnover (e.g., >50% replacement) only occurred when the selective advantage of the adaptive trait and translocation fraction were extremely high. Our results will be useful when adaptive management is used to maintain the genetic health and productivity of large populations under climate change.
Author Matthey‐Doret, Remi
Booker, Tom R.
Whitlock, Michael C.
Grummer, Jared A.
Nietlisbach, Pirmin
Thomaz, Andréa T.
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  surname: Whitlock
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Issue 4
Keywords local adaptation
migración latente
translocation
genética de la conservación
migration pulsing
reubicación
outbreeding depression
adaptación local
migración asistida
assisted migration
depresión exogámica
conservation genetics
Language English
License 2022 Society for Conservation Biology.
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Notes Jared A. Grummer, Tom R. Booker, Remi Matthey‐Doret, Pirmin Nietlisbach, and Andréa T. Thomaz contributed equally to this work.
Assisted gene flow can aid adaptation and improve the genetic health or fitness of a population, but usually the effect is small or delayed.
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Snippet With the genetic health of many plant and animal populations deteriorating due to climate change outpacing adaptation, interventions, such as assisted gene...
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SubjectTerms adaptación local
Adaptive management
Animal population
Animal populations
animals
assisted migration
Climate change
conservation genetics
depresión exogámica
Fitness
Gene flow
Genes
Genetic diversity
Genetic variation
Genomes
Genomics
Genotypes
genética de la conservación
Inbreeding
Inbreeding depression
local adaptation
migración asistida
migración latente
migration pulsing
Outbreeding
outbreeding depression
Population
Population genetics
Populations
Reproductive fitness
reubicación
Translocation
wildlife management
Title The immediate costs and long‐term benefits of assisted gene flow in large populations
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fcobi.13911
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