Genetics of dispersal

Marjo Saastamoinen, Greta Bocedi, Julien Cote, Delphine Legrand, Frédéric Guillaume, Christopher W Wheat, Emanuel A Fronhofer, Cristina Garcia, Roslyn Henry, Arild Husby, Michel Baguette, Dries Bonte, Aurélie Coulon, Hanna Kokko, Erik Matthysen, Kristjan Niitepõld, Etsuko Nonaka, Virginie M Stevens, Justin M J Travis, Kathleen Donohue & 2 others James M Bullock, Maria Del Mar Delgado

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Abstract

Dispersal is a process of central importance for the ecological and evolutionary dynamics of populations and communities, because of its diverse consequences for gene flow and demography. It is subject to evolutionary change, which begs the question, what is the genetic basis of this potentially complex trait? To address this question, we (i) review the empirical literature on the genetic basis of dispersal, (ii) explore how theoretical investigations of the evolution of dispersal have represented the genetics of dispersal, and (iii) discuss how the genetic basis of dispersal influences theoretical predictions of the evolution of dispersal and potential consequences. 


Dispersal has a detectable genetic basis in many organisms, from bacteria to plants and animals. Generally, there is evidence for significant genetic variation for dispersal or dispersal-related phenotypes or evidence for the micro-evolution of dispersal in natural populations. Dispersal is typically the outcome of several interacting traits, and this complexity is reflected in its genetic architecture: while some genes of moderate to large effect can influence certain aspects of dispersal, dispersal traits are typically polygenic. Correlations among dispersal traits as well as between dispersal traits and other traits under selection are common, and the genetic basis of dispersal can be highly environment-dependent. 


By contrast, models have historically considered a highly simplified genetic architecture of dispersal. It is only recently that models have started to consider multiple loci influencing dispersal, as well as non-additive effects such as dominance and epistasis, showing that the genetic basis of dispersal can influence evolutionary rates and outcomes, especially under non-equilibrium conditions. For example, the number of loci controlling dispersal can influence projected rates of dispersal evolution during range shifts and corresponding demographic impacts. Incorporating more realism in the genetic architecture of dispersal is thus necessary to enable models to move beyond the purely theoretical towards making more useful predictions of evolutionary and ecological dynamics under current and future environmental conditions. To inform these advances, empirical studies need to answer outstanding questions concerning whether specific genes underlie dispersal variation, the genetic architecture of context-dependent dispersal phenotypes and behaviours, and correlations among dispersal and other traits.

Original languageEnglish
Pages (from-to)574-599
Number of pages26
JournalBiological Reviews
Volume93
Issue number1
Early online date3 Aug 2017
DOIs
Publication statusPublished - Feb 2018

Fingerprint

Genetic Epistasis
Genes
Demography
Multifactorial Inheritance
Phenotype
Gene Flow
Population Dynamics
Bacteria
Animals
Population
Genetics
phenotype
genetic variation
loci
prediction
epistasis
demography
dominance (genetics)
gene flow
population dynamics

Keywords

  • dispersal kernel
  • eco-evolutionary models
  • gene flow
  • genetic architecture
  • genotype–environment interactions
  • heritability
  • life-history traits
  • migration
  • mobility
  • movement

Cite this

Saastamoinen, M., Bocedi, G., Cote, J., Legrand, D., Guillaume, F., Wheat, C. W., ... Del Mar Delgado, M. (2018). Genetics of dispersal. Biological Reviews, 93(1), 574-599. https://doi.org/10.1111/brv.12356

Genetics of dispersal. / Saastamoinen, Marjo; Bocedi, Greta; Cote, Julien; Legrand, Delphine; Guillaume, Frédéric; Wheat, Christopher W; Fronhofer, Emanuel A; Garcia, Cristina; Henry, Roslyn; Husby, Arild; Baguette, Michel; Bonte, Dries; Coulon, Aurélie; Kokko, Hanna; Matthysen, Erik; Niitepõld, Kristjan; Nonaka, Etsuko; Stevens, Virginie M; Travis, Justin M J; Donohue, Kathleen; Bullock, James M; Del Mar Delgado, Maria.

In: Biological Reviews, Vol. 93, No. 1, 02.2018, p. 574-599.

Research output: Contribution to journalArticle

Saastamoinen, M, Bocedi, G, Cote, J, Legrand, D, Guillaume, F, Wheat, CW, Fronhofer, EA, Garcia, C, Henry, R, Husby, A, Baguette, M, Bonte, D, Coulon, A, Kokko, H, Matthysen, E, Niitepõld, K, Nonaka, E, Stevens, VM, Travis, JMJ, Donohue, K, Bullock, JM & Del Mar Delgado, M 2018, 'Genetics of dispersal', Biological Reviews, vol. 93, no. 1, pp. 574-599. https://doi.org/10.1111/brv.12356
Saastamoinen M, Bocedi G, Cote J, Legrand D, Guillaume F, Wheat CW et al. Genetics of dispersal. Biological Reviews. 2018 Feb;93(1):574-599. https://doi.org/10.1111/brv.12356
Saastamoinen, Marjo ; Bocedi, Greta ; Cote, Julien ; Legrand, Delphine ; Guillaume, Frédéric ; Wheat, Christopher W ; Fronhofer, Emanuel A ; Garcia, Cristina ; Henry, Roslyn ; Husby, Arild ; Baguette, Michel ; Bonte, Dries ; Coulon, Aurélie ; Kokko, Hanna ; Matthysen, Erik ; Niitepõld, Kristjan ; Nonaka, Etsuko ; Stevens, Virginie M ; Travis, Justin M J ; Donohue, Kathleen ; Bullock, James M ; Del Mar Delgado, Maria. / Genetics of dispersal. In: Biological Reviews. 2018 ; Vol. 93, No. 1. pp. 574-599.
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abstract = "Dispersal is a process of central importance for the ecological and evolutionary dynamics of populations and communities, because of its diverse consequences for gene flow and demography. It is subject to evolutionary change, which begs the question, what is the genetic basis of this potentially complex trait? To address this question, we (i) review the empirical literature on the genetic basis of dispersal, (ii) explore how theoretical investigations of the evolution of dispersal have represented the genetics of dispersal, and (iii) discuss how the genetic basis of dispersal influences theoretical predictions of the evolution of dispersal and potential consequences. Dispersal has a detectable genetic basis in many organisms, from bacteria to plants and animals. Generally, there is evidence for significant genetic variation for dispersal or dispersal-related phenotypes or evidence for the micro-evolution of dispersal in natural populations. Dispersal is typically the outcome of several interacting traits, and this complexity is reflected in its genetic architecture: while some genes of moderate to large effect can influence certain aspects of dispersal, dispersal traits are typically polygenic. Correlations among dispersal traits as well as between dispersal traits and other traits under selection are common, and the genetic basis of dispersal can be highly environment-dependent. By contrast, models have historically considered a highly simplified genetic architecture of dispersal. It is only recently that models have started to consider multiple loci influencing dispersal, as well as non-additive effects such as dominance and epistasis, showing that the genetic basis of dispersal can influence evolutionary rates and outcomes, especially under non-equilibrium conditions. For example, the number of loci controlling dispersal can influence projected rates of dispersal evolution during range shifts and corresponding demographic impacts. Incorporating more realism in the genetic architecture of dispersal is thus necessary to enable models to move beyond the purely theoretical towards making more useful predictions of evolutionary and ecological dynamics under current and future environmental conditions. To inform these advances, empirical studies need to answer outstanding questions concerning whether specific genes underlie dispersal variation, the genetic architecture of context-dependent dispersal phenotypes and behaviours, and correlations among dispersal and other traits.",
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note = "M. S. thanks the European Research Council (IndependentStarting grant META-STRESS; 637412) and Academyof Finland (Decision numbers 273098 & 265461) forfunding. M. M. D. was supported by Ministeriode Economia y Competitividad ‘‘Ram´on y Cajalprogram’’ grant contract no. RYC-2014-16263. D. B.,E.A.F.,J.M.J.T.andE.M.arefundedby the FWO research community EVENET. D. B.is funded by FWO research grant INVADED G.018017.N.D. L., J. C., V. M. S. and M. B. are part of the Laboratoired’Excellence (LABEX) entitled TULIP (ANR-10-LABX-41).D. L. thanks Fyssen foundation for research funding.J. C. thanks an ANR-12-JSV7-0004-01. F. G. is supportedby SNSF grant PP00P3_144846. E. N. is supported byan International postdoctoral fellowship from the SwedishResearch Council (Vetenskapsr˚adet). E. A. F. thanks Eawagfor funding. J. M. B. thanks CEH for funding under projectNEC05264. C. G. thanks FCT (Fundac¸˜ao para a Ciencia e aTecnologia) for funding (FCT-ANR/BIA-BIC/0010/2013and IF Fellowship). M. B. and A. C. thank the ANRfor funding (INDHET program, ANR-12-BSV7-0023).V. M. S. thanks the ANR for funding (GEMS programANR-13-JSV7-0010-01). K. N. thanks the Ella and GeorgEhrnrooth Foundation and the Emil Aaltonen Foundationfor funding. E. M. is supported by UA-TOPBOF andFWO-project G030813N.",
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AU - Cote, Julien

AU - Legrand, Delphine

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AU - Wheat, Christopher W

AU - Fronhofer, Emanuel A

AU - Garcia, Cristina

AU - Henry, Roslyn

AU - Husby, Arild

AU - Baguette, Michel

AU - Bonte, Dries

AU - Coulon, Aurélie

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AU - Niitepõld, Kristjan

AU - Nonaka, Etsuko

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AU - Travis, Justin M J

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AU - Bullock, James M

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N2 - Dispersal is a process of central importance for the ecological and evolutionary dynamics of populations and communities, because of its diverse consequences for gene flow and demography. It is subject to evolutionary change, which begs the question, what is the genetic basis of this potentially complex trait? To address this question, we (i) review the empirical literature on the genetic basis of dispersal, (ii) explore how theoretical investigations of the evolution of dispersal have represented the genetics of dispersal, and (iii) discuss how the genetic basis of dispersal influences theoretical predictions of the evolution of dispersal and potential consequences. Dispersal has a detectable genetic basis in many organisms, from bacteria to plants and animals. Generally, there is evidence for significant genetic variation for dispersal or dispersal-related phenotypes or evidence for the micro-evolution of dispersal in natural populations. Dispersal is typically the outcome of several interacting traits, and this complexity is reflected in its genetic architecture: while some genes of moderate to large effect can influence certain aspects of dispersal, dispersal traits are typically polygenic. Correlations among dispersal traits as well as between dispersal traits and other traits under selection are common, and the genetic basis of dispersal can be highly environment-dependent. By contrast, models have historically considered a highly simplified genetic architecture of dispersal. It is only recently that models have started to consider multiple loci influencing dispersal, as well as non-additive effects such as dominance and epistasis, showing that the genetic basis of dispersal can influence evolutionary rates and outcomes, especially under non-equilibrium conditions. For example, the number of loci controlling dispersal can influence projected rates of dispersal evolution during range shifts and corresponding demographic impacts. Incorporating more realism in the genetic architecture of dispersal is thus necessary to enable models to move beyond the purely theoretical towards making more useful predictions of evolutionary and ecological dynamics under current and future environmental conditions. To inform these advances, empirical studies need to answer outstanding questions concerning whether specific genes underlie dispersal variation, the genetic architecture of context-dependent dispersal phenotypes and behaviours, and correlations among dispersal and other traits.

AB - Dispersal is a process of central importance for the ecological and evolutionary dynamics of populations and communities, because of its diverse consequences for gene flow and demography. It is subject to evolutionary change, which begs the question, what is the genetic basis of this potentially complex trait? To address this question, we (i) review the empirical literature on the genetic basis of dispersal, (ii) explore how theoretical investigations of the evolution of dispersal have represented the genetics of dispersal, and (iii) discuss how the genetic basis of dispersal influences theoretical predictions of the evolution of dispersal and potential consequences. Dispersal has a detectable genetic basis in many organisms, from bacteria to plants and animals. Generally, there is evidence for significant genetic variation for dispersal or dispersal-related phenotypes or evidence for the micro-evolution of dispersal in natural populations. Dispersal is typically the outcome of several interacting traits, and this complexity is reflected in its genetic architecture: while some genes of moderate to large effect can influence certain aspects of dispersal, dispersal traits are typically polygenic. Correlations among dispersal traits as well as between dispersal traits and other traits under selection are common, and the genetic basis of dispersal can be highly environment-dependent. By contrast, models have historically considered a highly simplified genetic architecture of dispersal. It is only recently that models have started to consider multiple loci influencing dispersal, as well as non-additive effects such as dominance and epistasis, showing that the genetic basis of dispersal can influence evolutionary rates and outcomes, especially under non-equilibrium conditions. For example, the number of loci controlling dispersal can influence projected rates of dispersal evolution during range shifts and corresponding demographic impacts. Incorporating more realism in the genetic architecture of dispersal is thus necessary to enable models to move beyond the purely theoretical towards making more useful predictions of evolutionary and ecological dynamics under current and future environmental conditions. To inform these advances, empirical studies need to answer outstanding questions concerning whether specific genes underlie dispersal variation, the genetic architecture of context-dependent dispersal phenotypes and behaviours, and correlations among dispersal and other traits.

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KW - eco-evolutionary models

KW - gene flow

KW - genetic architecture

KW - genotype–environment interactions

KW - heritability

KW - life-history traits

KW - migration

KW - mobility

KW - movement

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