Abstract
It has been proposed that inbreeding contributes to the decline and eventual extinction of small and isolated populations1,2. There is ample evidence of fitness reduction due to inbreeding (inbreeding depression) in captivity3,4,5,6,7 and from a few experimental8,9 and observational field studies10,11, but no field studies on natural populations have been conducted to test the proposed effect on extinction. It has been argued that in natural populations the impact of inbreeding depression on population survival will be insignificant in comparison to that of demographic and environmental stochasticity12,13. We have now studied the effect of inbreeding on local extinction in a large metapopulation14 of the Glanville fritillary butterfly (Melitaea cinxia)15. We found that extinction risk increased significantly with decreasing heterozygosity, an indication of inbreeding6, even after accounting for the effects of the relevant ecological factors. Larval survival, adult longevity and egg-hatching rate were found to be adversely affected by inbreeding and appear to be the fitness components underlying the relationship between inbreeding and extinction. To our knowledge, this is the first demonstration of an effect of inbreeding on the extinction of natural populations. Our results are particularly relevant to the increasing number of species with small local populations due to habitat loss and fragmentation16.
Your institute does not have access to this article
Relevant articles
Open Access articles citing this article.
-
Inbreeding is associated with shorter early-life telomere length in a wild passerine
Conservation Genetics Open Access 10 April 2022
-
Gene-flow within a butterfly metapopulation: the marsh fritillary Euphydryas aurinia in western Bohemia (Czech Republic)
Journal of Insect Conservation Open Access 06 June 2021
-
Population genomics and conservation management of a declining tropical rodent
Heredity Open Access 04 March 2021
Access options
Subscribe to Journal
Get full journal access for 1 year
$199.00
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Buy article
Get time limited or full article access on ReadCube.
$32.00
All prices are NET prices.


References
Frankham, R. Conservation genetics. Annu. Rev. Genet. 29, 305–327 (1995).
Frankham, R. Inbreeding and extinction: a threshold effect. Conserv. Biol. 9, 792–799 (1995).
Charlesworth, D. & Charlesworth, B. Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18, 237–268 (1987).
Ralls, K., Ballou, J. D. & Templeton, A. Estimates of lethal equivalents and the cost of inbreeding in mammals. Conserv. Biol. 2, 185–193 (1988).
Thornhill, N. W. (ed.) The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives (University of Chicago Press, Chicago, (1993)).
Falconer, D. S. & Mackay, T. F. C. Introduction to Quantitative Genetics4th edn (Longman, Burnt Mill, Harlow, UK, (1996)).
Saccheri, I. J., Brakefield, P. M. & Nichols, R. A. Severe inbreeding and rapid fitness rebound in the butterfly Bicyclus anynana (Satyridae). Evolution 50, 2000–2013 (1996).
Jiménez, J. A., Hughes, K. A., Alaks, G., Graham, L. & Lacy, R. C. An experimental study of inbreeding depression in a natural habitat. Science 266, 271–273 (1994).
Newman, D. & Pilson, D. Increased probability of extinction due to decreased effective population size: experimental populations of Clarkia pulchella. Evolution 51, 354–362 (1997).
Keller, L. F., Arcese, P., Smith, J. N. M., Hochachka, W. M. & Stearns, S. C. Selection against inbred song sparrows during a natural population bottleneck. Nature 372, 356–357 (1994).
Madsen, T., Stille, B. & Shine, R. Inbreeding depression in an isolated population of adders Vipera berus. Biol. Conserv. 75, 113–118 (1996).
Caro, T. M. & Laurenson, M. K. Ecological and genetic factors in conservation: a cautionary tale. Science 263, 485–486 (1994).
Caughley, G. Directions in conservation biology. Anim. Ecol. 63, 215–244 (1994).
Hanski, I. A. & Gilpin, M. E. (eds) Metapopulation Biology: Ecology, Genetics, and Evolution (Academic, San Diego, (1997)).
Hanski, I., Pakkala, T., Kuussaari, M. & Lei, G. Metapopulation persistence of an endangered butterfly in a fragmented landscape. Oikos 72, 21–28 (1995).
Lande, R. Genetics and demography in biological conservation. Science 241, 1455–1460 (1988).
Hanski, I., Pöyry, J., Pakkala, T. & Kuussaari, M. Multiple equilibria in metapopulation dynamics. Nature 377, 618–621 (1995).
Hanski, I., Moilanen, A., Pakkala, T. & Kuussaari, M. The quantitative incidence function model and persistence of an endangered butterfly metapopulation. Conserv. Biol. 10, 578–590 (1996).
Hanski, I. Apractical model of metapopulation dynamics. Anim. Ecol. 63, 151–162 (1994).
Hanski, I. Metapopulation dynamics: from concepts and observations to predictive models in Metapopulation Biology: Ecology, Genetics, and Evolution(eds Hanski, I. A. & Gilpin, M. E.) 69–91 (Academic, San Diego, (1997)).
Hanski, I., Kuussaari, M. & Nieminen, M. Metapopulation structure and migration in the butterfly Melitaea cinxia. Ecology 75, 747–762 (1994).
Lei, G. C. & Hanski, I. Metapopulation structure of Cotesia melitaearum, a specialist parasitoid of the butterfly, Melitaea cinxia. Oikos 78, 91–100 (1997).
Kuussaari, M., Nieminen, M. & Hanski, I. An experimental study of migration in the Glanville fritillary butterfly Melitaea cinxia. J. Anim. Ecol. 65, 791–801 (1996).
Lei, G. C., Vikberg, V., Nieminen, M. & Kuussaari, M. The parasitoid complex attacking Finnish populations of the Glanville fritillary Melitaea cinxia (Lep: Nymphalidae), an endangered butterfly. J. Nat. Hist. 31, 635–648 (1997).
Wahlberg, N. One Day in the Life of a Butterfly; a Study of the Glanville Fritillary Melitaea cinxia (Thesis, Univ. Helsinki, (1995)).
Hedrick, P. W. Purging inbreeding depression and the probability of extinction: full-sib mating. Heredity 73, 363–372 (1994).
Lynch, M., Conery, J. & Bürger, R. Mutation accumulation and the extinction of small populations. Am. Nat. 146, 489–518 (1995).
Acknowledgements
We thank K. Higgins, L. Keller, R. Lande, M. Lynch, A. Moilanen, R. Nichols, S. van Nouhuys, M. Singer and C. Thomas for their helpful comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Saccheri, I., Kuussaari, M., Kankare, M. et al. Inbreeding and extinction in a butterfly metapopulation. Nature 392, 491–494 (1998). https://doi.org/10.1038/33136
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/33136
Further reading
-
Research Progress on endangered plants: a bibliometric analysis
Biodiversity and Conservation (2022)
-
Inbreeding is associated with shorter early-life telomere length in a wild passerine
Conservation Genetics (2022)
-
DNA matchmaking in captive facilities: a case study with tigers
Molecular Biology Reports (2022)
-
Riverscape genetics in brook lamprey: genetic diversity is less influenced by river fragmentation than by gene flow with the anadromous ecotype
Heredity (2021)
-
Population genomics and conservation management of a declining tropical rodent
Heredity (2021)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.