A systematic review of phenotypic responses to between-population outbreeding

Raj Whitlock* (Corresponding Author), Gavin B. Stewart, Simon J. Goodman, Stuart B. Piertney, Roger K. Butlin, Andrew S. Pullin, Terry Burke

*Corresponding author for this work

Research output: Contribution to journalArticle

18 Citations (Scopus)
4 Downloads (Pure)

Abstract

Background: The translocation of plants or animals between populations has been used in conservation to reinforce populations of threatened species, and may be used in the future to buffer species' ranges from the anticipated effects of environmental change. This population admixture can result in outbreeding, and the resulting "hybrid" offspring can be either fitter (heterosis) or less fit (outbreeding depression) than their parents. Outbreeding depression has the potential to undermine conservation plans that mix populations of declining or threatened species. Methods: We searched for literature documenting phenotypic responses to intraspecific outbreeding between natural populations of animal and plant species. Outbreeding responses were summarised as log-response ratios that compared hybrid with mid-parent phenotypes (528 effect sizes from 98 studies). These data included effect sizes from both fitness components (survival, viability and fecundity traits) and other traits (e.g. morphological, physiological, defence), and were pooled using Bayesian mixed-effects meta-analysis. Results: There was no overall effect of outbreeding on hybrid phenotypes (overall pooled effect = +2.61% phenotypic change relative to parents, 95% credible interval (CI) -1.03-6.60%). However, fitness component traits responded significantly more negatively to outbreeding than traits less directly linked with fitness. Our model predicted a significant 6.9% F1 generation benefit to outcrossing through non-fitness traits (CI 2.7-11.2%), but no significant benefit to these traits in the F2 (3.5%; CI -4.3-12.2%). Fitness component traits were predicted to suffer a cost (-8.8%) relative to parents in the F2 (CI -14.1- - 2.5%), but not in the F1 (+1.3%; CI -2.1-5.4%). Between-study variation accounted for 39.5% of heterogeneity in outbreeding responses, leaving 27.1% of heterogeneity between effect sizes within studies and 33.4% attributable to measurement error within effect sizes. Conclusions: Our study demonstrates consistent effects of trait type on responses to intraspecific outbreeding, and indicates the potential for outbreeding depression in the F2. However, our analyses also reveal significant heterogeneity in outbreeding responses within and among studies. Thus, outbreeding costs will not always occur. Conservation practitioners may be able to anticipate when such outbreeding depression should arise using an existing decision-making framework that takes into account the context of hybridising populations.

Original languageEnglish
Article number13
JournalEnvironmental Evidence
Volume2
DOIs
Publication statusPublished - 26 Jun 2013

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Conservation
Animals
fitness
Measurement errors
Costs
Decision making
phenotype
effect
heterosis
outcrossing
meta-analysis
cost
translocation
fecundity
environmental change
viability
decision making

Keywords

  • Conservation Genetics
  • Heterosis
  • Intraspecific Hybridisation
  • Line-cross Analysis
  • Outbreeding
  • Outbreeding Depression
  • Outcrossing
  • Phenotypic Response

ASJC Scopus subject areas

  • Ecology
  • Pollution
  • Management, Monitoring, Policy and Law

Cite this

Whitlock, R., Stewart, G. B., Goodman, S. J., Piertney, S. B., Butlin, R. K., Pullin, A. S., & Burke, T. (2013). A systematic review of phenotypic responses to between-population outbreeding. Environmental Evidence, 2, [13]. https://doi.org/10.1186/2047-2382-2-13

A systematic review of phenotypic responses to between-population outbreeding. / Whitlock, Raj (Corresponding Author); Stewart, Gavin B.; Goodman, Simon J.; Piertney, Stuart B.; Butlin, Roger K.; Pullin, Andrew S.; Burke, Terry.

In: Environmental Evidence, Vol. 2, 13, 26.06.2013.

Research output: Contribution to journalArticle

Whitlock, Raj ; Stewart, Gavin B. ; Goodman, Simon J. ; Piertney, Stuart B. ; Butlin, Roger K. ; Pullin, Andrew S. ; Burke, Terry. / A systematic review of phenotypic responses to between-population outbreeding. In: Environmental Evidence. 2013 ; Vol. 2.
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title = "A systematic review of phenotypic responses to between-population outbreeding",
abstract = "Background: The translocation of plants or animals between populations has been used in conservation to reinforce populations of threatened species, and may be used in the future to buffer species' ranges from the anticipated effects of environmental change. This population admixture can result in outbreeding, and the resulting {"}hybrid{"} offspring can be either fitter (heterosis) or less fit (outbreeding depression) than their parents. Outbreeding depression has the potential to undermine conservation plans that mix populations of declining or threatened species. Methods: We searched for literature documenting phenotypic responses to intraspecific outbreeding between natural populations of animal and plant species. Outbreeding responses were summarised as log-response ratios that compared hybrid with mid-parent phenotypes (528 effect sizes from 98 studies). These data included effect sizes from both fitness components (survival, viability and fecundity traits) and other traits (e.g. morphological, physiological, defence), and were pooled using Bayesian mixed-effects meta-analysis. Results: There was no overall effect of outbreeding on hybrid phenotypes (overall pooled effect = +2.61{\%} phenotypic change relative to parents, 95{\%} credible interval (CI) -1.03-6.60{\%}). However, fitness component traits responded significantly more negatively to outbreeding than traits less directly linked with fitness. Our model predicted a significant 6.9{\%} F1 generation benefit to outcrossing through non-fitness traits (CI 2.7-11.2{\%}), but no significant benefit to these traits in the F2 (3.5{\%}; CI -4.3-12.2{\%}). Fitness component traits were predicted to suffer a cost (-8.8{\%}) relative to parents in the F2 (CI -14.1- - 2.5{\%}), but not in the F1 (+1.3{\%}; CI -2.1-5.4{\%}). Between-study variation accounted for 39.5{\%} of heterogeneity in outbreeding responses, leaving 27.1{\%} of heterogeneity between effect sizes within studies and 33.4{\%} attributable to measurement error within effect sizes. Conclusions: Our study demonstrates consistent effects of trait type on responses to intraspecific outbreeding, and indicates the potential for outbreeding depression in the F2. However, our analyses also reveal significant heterogeneity in outbreeding responses within and among studies. Thus, outbreeding costs will not always occur. Conservation practitioners may be able to anticipate when such outbreeding depression should arise using an existing decision-making framework that takes into account the context of hybridising populations.",
keywords = "Conservation Genetics, Heterosis, Intraspecific Hybridisation, Line-cross Analysis, Outbreeding, Outbreeding Depression, Outcrossing, Phenotypic Response",
author = "Raj Whitlock and Stewart, {Gavin B.} and Goodman, {Simon J.} and Piertney, {Stuart B.} and Butlin, {Roger K.} and Pullin, {Andrew S.} and Terry Burke",
note = "This work was supported by the UK Population Biology Network, through funding from the Natural Environment Research Council and Natural England. We thank Jack Brodie, Helen Hipperson, Marie Chadburn and Sophie Allen for assistance with literature searching, article assessment and data extraction. We also thank our review group for constructive criticism on the scope, development and structure of this review, and two peer reviewers for useful feedback on the review protocol. Finally we thank three peer reviewers who each provided constructive comments on this systematic review report.",
year = "2013",
month = "6",
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doi = "10.1186/2047-2382-2-13",
language = "English",
volume = "2",
journal = "Environmental Evidence",
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TY - JOUR

T1 - A systematic review of phenotypic responses to between-population outbreeding

AU - Whitlock, Raj

AU - Stewart, Gavin B.

AU - Goodman, Simon J.

AU - Piertney, Stuart B.

AU - Butlin, Roger K.

AU - Pullin, Andrew S.

AU - Burke, Terry

N1 - This work was supported by the UK Population Biology Network, through funding from the Natural Environment Research Council and Natural England. We thank Jack Brodie, Helen Hipperson, Marie Chadburn and Sophie Allen for assistance with literature searching, article assessment and data extraction. We also thank our review group for constructive criticism on the scope, development and structure of this review, and two peer reviewers for useful feedback on the review protocol. Finally we thank three peer reviewers who each provided constructive comments on this systematic review report.

PY - 2013/6/26

Y1 - 2013/6/26

N2 - Background: The translocation of plants or animals between populations has been used in conservation to reinforce populations of threatened species, and may be used in the future to buffer species' ranges from the anticipated effects of environmental change. This population admixture can result in outbreeding, and the resulting "hybrid" offspring can be either fitter (heterosis) or less fit (outbreeding depression) than their parents. Outbreeding depression has the potential to undermine conservation plans that mix populations of declining or threatened species. Methods: We searched for literature documenting phenotypic responses to intraspecific outbreeding between natural populations of animal and plant species. Outbreeding responses were summarised as log-response ratios that compared hybrid with mid-parent phenotypes (528 effect sizes from 98 studies). These data included effect sizes from both fitness components (survival, viability and fecundity traits) and other traits (e.g. morphological, physiological, defence), and were pooled using Bayesian mixed-effects meta-analysis. Results: There was no overall effect of outbreeding on hybrid phenotypes (overall pooled effect = +2.61% phenotypic change relative to parents, 95% credible interval (CI) -1.03-6.60%). However, fitness component traits responded significantly more negatively to outbreeding than traits less directly linked with fitness. Our model predicted a significant 6.9% F1 generation benefit to outcrossing through non-fitness traits (CI 2.7-11.2%), but no significant benefit to these traits in the F2 (3.5%; CI -4.3-12.2%). Fitness component traits were predicted to suffer a cost (-8.8%) relative to parents in the F2 (CI -14.1- - 2.5%), but not in the F1 (+1.3%; CI -2.1-5.4%). Between-study variation accounted for 39.5% of heterogeneity in outbreeding responses, leaving 27.1% of heterogeneity between effect sizes within studies and 33.4% attributable to measurement error within effect sizes. Conclusions: Our study demonstrates consistent effects of trait type on responses to intraspecific outbreeding, and indicates the potential for outbreeding depression in the F2. However, our analyses also reveal significant heterogeneity in outbreeding responses within and among studies. Thus, outbreeding costs will not always occur. Conservation practitioners may be able to anticipate when such outbreeding depression should arise using an existing decision-making framework that takes into account the context of hybridising populations.

AB - Background: The translocation of plants or animals between populations has been used in conservation to reinforce populations of threatened species, and may be used in the future to buffer species' ranges from the anticipated effects of environmental change. This population admixture can result in outbreeding, and the resulting "hybrid" offspring can be either fitter (heterosis) or less fit (outbreeding depression) than their parents. Outbreeding depression has the potential to undermine conservation plans that mix populations of declining or threatened species. Methods: We searched for literature documenting phenotypic responses to intraspecific outbreeding between natural populations of animal and plant species. Outbreeding responses were summarised as log-response ratios that compared hybrid with mid-parent phenotypes (528 effect sizes from 98 studies). These data included effect sizes from both fitness components (survival, viability and fecundity traits) and other traits (e.g. morphological, physiological, defence), and were pooled using Bayesian mixed-effects meta-analysis. Results: There was no overall effect of outbreeding on hybrid phenotypes (overall pooled effect = +2.61% phenotypic change relative to parents, 95% credible interval (CI) -1.03-6.60%). However, fitness component traits responded significantly more negatively to outbreeding than traits less directly linked with fitness. Our model predicted a significant 6.9% F1 generation benefit to outcrossing through non-fitness traits (CI 2.7-11.2%), but no significant benefit to these traits in the F2 (3.5%; CI -4.3-12.2%). Fitness component traits were predicted to suffer a cost (-8.8%) relative to parents in the F2 (CI -14.1- - 2.5%), but not in the F1 (+1.3%; CI -2.1-5.4%). Between-study variation accounted for 39.5% of heterogeneity in outbreeding responses, leaving 27.1% of heterogeneity between effect sizes within studies and 33.4% attributable to measurement error within effect sizes. Conclusions: Our study demonstrates consistent effects of trait type on responses to intraspecific outbreeding, and indicates the potential for outbreeding depression in the F2. However, our analyses also reveal significant heterogeneity in outbreeding responses within and among studies. Thus, outbreeding costs will not always occur. Conservation practitioners may be able to anticipate when such outbreeding depression should arise using an existing decision-making framework that takes into account the context of hybridising populations.

KW - Conservation Genetics

KW - Heterosis

KW - Intraspecific Hybridisation

KW - Line-cross Analysis

KW - Outbreeding

KW - Outbreeding Depression

KW - Outcrossing

KW - Phenotypic Response

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U2 - 10.1186/2047-2382-2-13

DO - 10.1186/2047-2382-2-13

M3 - Article

VL - 2

JO - Environmental Evidence

JF - Environmental Evidence

SN - 2047-2382

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