The fitness consequences of inbreeding in natural populations and their implications for species conservation – a systematic map

Environmental Evidence

Andrew S Pullin⁴  Terry Burke³  Peter M Hollingsworth¹  Raj Whitlock²  Jacqualyn Eales⁴  Linda E Neaves¹ 

[1] Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, UK;Institute of Integrative Biology, University of Liverpool, The Biosciences Building, Crown Street, Liverpool L69 7ZB, UK;Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK;Centre for Evidence-Based Conservation, School of Environment and Natural Resources and Geography, Bangor University, Bangor LL57 2UW, UK

关键词: Small populations;    Isolated populations;    Genetic load;    Heterosis;    Outbreeding;    Inbreeding depression;    Systematic review;    Conservation genetics;    Genetic variation;   

Others  :  1136291
DOI  :  10.1186/s13750-015-0031-x

 received in 2014-08-21, accepted in 2015-01-27,  发布年份 2015

【 摘 要 】

Background

Threatened species often have small and isolated populations where mating among relatives can result in inbreeding depression increasing extinction risk. Effective management is hampered by a lack of syntheses summarising the magnitude of, and variation in inbreeding depression. Here we describe the nature and scope of the literature examining phenotypic/fitness consequences of inbreeding, to provide a foundation for future syntheses and management.

Methods

We searched the literature for articles documenting the impact of inbreeding in natural populations. Article titles, abstracts and full-texts were assessed against a priori defined criteria, and information relating to study design, quality and other factors that may influence inbreeding responses (e.g. population size) was extracted from relevant articles.

Results

The searches identified 11457 articles, of which 614 were assessed as relevant and included in the systematic map (corresponding to 703 distinct studies). Most studies (663) assessed within-population inbreeding resulting from self-fertilisation or consanguineous pairings, while 118 studies assessed among-population inbreeding due to drift load. Plants were the most studied taxon (469 studies) followed by insects (52 studies) and birds (43 studies). Most studies investigated the effects of inbreeding on components of fitness (e.g. survival or fecundity; 648 studies) but measurements were typically under laboratory/greenhouse conditions (486 studies). Observations were also often restricted to the first inbred generation (607 studies) and studies frequently lacked contextual information (e.g. population size).

Conclusions

Our systematic map describes the scope and quality of the evidence describing the phenotypic consequences of inbreeding. The map reveals substantial evidence relating to inbreeding responses exists, but highlights information is still limited for some aspects, including the effects of multiple generations of inbreeding. The systematic map allowed us to define several conservation-relevant questions, where sufficient data exists to support systematic reviews, e.g. How do inbreeding responses vary with population size? However, we found that such syntheses are likely to be constrained by incomplete reporting of critical contextual information. Our systematic map employed the same rigorous literature assessment methods as systematic review, including a novel survey of study quality and thus provides a robust foundation to guide future research and syntheses seeking to inform conservation decision-making.

【 授权许可】

   
2015 Neaves et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Frankham R: Inbreeding in the wild really does matter. Heredity 2010, 104:124.
• [2]Keller LF, Waller DM: Inbreeding effects in wild populations. Trends Ecol Evol 2002, 17:230-41.
• [3]Spielman D, Brook BW, Frankham R: Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci U S A 2004, 101:15261-4.
• [4]Frankham R, Ballou JD, Briscoe DA: Introduction to Conservation Genetics. Cambridge University Press, Cambridge; 2010.
• [5]Charlesworth D, Willis JH: The genetics of inbreeding depression. Nat Rev Genet 2009, 10:783-96.
• [6]Charlesworth B, Charlesworth D: The genetic basis of inbreeding depression. Genet Res 1999, 74:329-40.
• [7]Hedrick PW, Adams JR, Vucetich JA: Reevaluating and broadening the definition of genetic rescue. Conserv Biol 2011, 25:1069-70.
• [8]Hedrick P, Fredrickson R: Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conserv Genet 2010, 11:615-26.
• [9]Johnson WE, Onorato DP, Roelke ME, Land ED, Cunningham M, Belden RC, et al.: Genetic restoration of the Florida panther. Science 2010, 329:1641-5.
• [10]Madsen T, Ujvari B, Olsson M: Novel genes continue to enhance population growth in adders (Vipera berus). Biol Conserv 2004, 120:145-7.
• [11]Madsen T, Shine R, Olsson M, Wittzell H: Conservation Biology: restoration of an inbred adder population. Nature 1999, 402:34-5.
• [12]Willi Y, van Kleunen M, Dietrich S, Fischer M: Genetic rescue persists beyond first-generation outbreeding in small populations of a rare plant. Proc R Soc B Biol Sci 2007, 274:2357-64.
• [13]Edmands S: Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 2007, 16:463-75.
• [14]Lynch M: The genetic interpretation of inbreeding depression and outbreeding depression. Evolution 1991, 45:622-9.
• [15]Whitlock R, Stewart GB, Goodman SJ, Piertney SB, Butlin RK, Pullin A, et al.: A systematic review of phenotypic responses to between-population outbreeding. Environ Evid 2013, 2:13. BioMed Central Full Text
• [16]Frankham R, Ballou JD, Eldridge MDB, Lacy RC, Ralls K, Dudash MR, et al.: Predicting the probability of outbreeding depression. Conserv Biol 2011, 25:465-75.
• [17]Hedrick PW, Kalinowski ST: Inbreeding depression in conservation biology. Annu Rev Ecol Syst 2000, 31:139-62.
• [18]Crnokrak P, Roff DA: Inbreeding depression in the wild. Heredity (Edinb) 1999, 83:260-70.
• [19]O’Grady JJ, Brook BW, Reed DH, Ballou JD, Tonkyn DW, Frankham R: Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biol Conserv 2006, 133:42-51.
• [20]Angeloni F, Ouborg NJ, Leimu R: Meta-analysis on the association of population size and life history with inbreeding depression in plants. Biol Conserv 2011, 144:35-43.
• [21]Fox CW, Reed DH: Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution 2011, 65:246-58.
• [22]Grant MJ, Booth A: A typology of reviews: an analysis of 14 review types and associated methodologies. Heal Inf Libr J 2009, 26:91-108.
• [23]Fay MF, Sutcliffe J, Jones B, Taylor I: Proceedings of a Conservation Genetics Workshop Held at the Royal Botanic Gardens, Kew. 2001.
• [24]Ferris R: Research Needs for UK Biodiversity. DEFRA, London; 2007.
• [25]Gregory A, Burke T, Ferris T, Robson J, Smithers R, Whitlock R: The conservation of genetic diversity: science and policy needs in a changing world. 2006.
• [26]Collaboration for Environmental Evidence. Guidelines for systematic review and evidence synthesis in environmental management. version 4.2. 2013. Environmental Evidence: www.environmentalevidence.org/wp-content/uploads/2014/06/Review-guidelines-version-4.2-final.pdf.
• [27]Whitlock R, Eales J, Chadburn M, Neaves LE, Hollingsworth PM, Burke T, Pullin AS. How do species’ characteristics influence the cost of inbreeding? CEE Protocol 10-014. Collaboration for Environmental Evidence. 2012. http://www.environmentalevidence.org/wp-content/uploads/2014/06/Protocol10-014.pdf.
• [28]Randall N, James K: The effectiveness of integrated farm management, organic farming and agri-environment schemes for conserving biodiversity in temperate Europe - a systematic map. Environ Evid 2012, 1:4. BioMed Central Full Text
• [29]Cohen JE: A coefficient of agreement for nominal scales. Educ Psychol Meas 1960, 30:37-46.
• [30]Landis JR, Koch GG: The measurement of observer agreement for categorical data. Biometrics 1977, 33:159-74.
• [31]Lande R: Genetics and demography in biological conservation. Science 1988, 241:1455-60.
• [32]Caughley G: Directions in conservation biology. J Anim Ecol 1994, 63:215-44.
• [33]Ralls K, Ballou JD, Templeton A: Estimates of lethal equivalents and the cost of inbreeding in mammals. Conserv Biol 1988, 2:185-93.
• [34]Theodorou K, Couvet D: On the expected relationship between inbreeding, fitness, and extinction. Genet Sel Evol 2006, 38:371-87. BioMed Central Full Text
• [35]Larsen LK, PeLabon C, Bolstad GH, Viken Å, Fleming IA, Rosenqvist G: Temporal change in inbreeding depression in life-history traits in captive populations of guppy (Poecilia reticulata): evidence for purging? J Evol Biol 2011, 24:823-34.
• [36]Pekkala N, Emily Knott K, Kotiaho JS, Puurtinen M: Inbreeding rate modifies the dynamics of genetic load in small populations. Ecol Evol 2012, 2:1791-804.
• [37]Crnokrak P, Barrett SCH: Perspective: purging the genetic load: a review of the experimental evidence. Evolution 2002, 56:2347-58.
• [38]Byers DL, Waller DM: Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annu Rev Ecol Syst 1999, 30:479-513.
• [39]Reed DH, Fox CW, Enders LS, Kristensen TN: Inbreeding–stress interactions: evolutionary and conservation consequences. Ann N Y Acad Sci 2012, 1256:33-48.
• [40]Nielsen JF, English S, Goodall-Copestake WP, Wang J, Walling CA, Bateman AW, et al.: Inbreeding and inbreeding depression of early life traits in a cooperative mammal. Mol Ecol 2012, 21:2788-804.
• [41]Brekke P, Bennett PM, Wang J, Pettorelli N, Ewen JG: Sensitive males: inbreeding depression in an endangered bird. Proc R Soc B Biol Sci 2010, 277:3677-84.
• [42]Castellanos M, Verdú M: Meta-analysis of meta-analyses in plant evolutionary ecology. Evol Ecol 2012, 26:1187-96.
• [43]Reed DH, Frankham R: Correlation between fitness and genetic diversity. Conserv Biol 2003, 17:230-7.
• [44]Leimu R, Mutikainen PIA, Koricheva J, Fischer M: How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 2006, 94:942-52.
• [45]Reed DH, Frankham R: How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 2001, 55:1095-103.
• [46]Frankham R: Effective population size/adult population size ratios in wildlife: a review. Genet Res 1995, 66:95-107.
• [47]Wright S: The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 1965, 19:395-420.