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Multiple life-stage inbreeding depression impacts demography and extinction risk in an extinct-in-the-wild species

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  • 1.

    Keller, L. F. & Waller, D. M. Inbreeding effects in wild populations. Trends Ecol. Evol. 17, 230–241 (2002).

    Article  Google Scholar 

  • 2.

    Boakes, E. H., Wang, J. & Amos, W. An investigation of inbreeding depression and purging in captive pedigreed populations. Heredity (Edinb). 98, 172–182 (2007).

    CAS  PubMed  Article  Google Scholar 

  • 3.

    Bozzuto, C., Biebach, I., Muff, S., Ives, A. R. & Keller, L. F. Inbreeding reduces long-term growth of Alpine ibex populations. Nat. Ecol. Evol. 3, 1359–1364 (2019).

    PubMed  Article  Google Scholar 

  • 4.

    Saccheri, I., Kuussaari, M., Kankare, M., Vikman, P. & Hanski, I. Inbreeding and extinction in a butterfly metapopulation. Nature 392, 491–494 (1998).

    ADS  CAS  Article  Google Scholar 

  • 5.

    Kardos, M., Taylor, H. R., Ellegren, H., Luikart, G. & Allendorf, F. W. Genomics advances the study of inbreeding depression in the wild. Evol. Appl. 9, 1205–1218 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  • 6.

    Allendorf, F. W., Luikart, G. & Aitken, S. N. Conservation and the genetics of populations. (Wiley-Blackwell, 2013).

  • 7.

    Johnson, H. E., Mills, L. S., Wehausen, J. D., Stephenson, T. R. & Luikart, G. Translating effects of inbreeding depression on component vital rates to overall population growth in endangered bighorn sheep. Conserv. Biol. 25, 1240–1249 (2011).

    PubMed  Article  Google Scholar 

  • 8.

    Frankham, R. Where are we in conservation genetics and where do we need to go?. Conserv. Genet. 11, 661–663 (2010).

    Article  Google Scholar 

  • 9.

    Pierson, J. C. et al. Incorporating evolutionary processes into population viability models. Conserv. Biol. 29, 755–764 (2015).

    PubMed  Article  Google Scholar 

  • 10.

    Huisman, J., Kruuk, L. E. B., Ellisa, P. A., Clutton-Brock, T. & Pemberton, J. M. Inbreeding depression across the lifespan in a wild mammal population. Proc. Natl. Acad. Sci. U. S. A. 113, 3585–3590 (2016).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 11.

    Grueber, C. E., Laws, R. J., Nakagawa, S. & Jamieson, I. G. Inbreeding depression accumulation across life-history stages of the endangered takahe. Conserv. Biol. 24, 1617–1625 (2010).

    PubMed  Article  Google Scholar 

  • 12.

    Harrisson, K. A. et al. Lifetime fitness costs of inbreeding and being inbred in a critically endangered bird. Curr. Biol. 29, 2711-2717.e4 (2019).

    CAS  PubMed  Article  Google Scholar 

  • 13.

    Ralls, K., Ballou, J. D. & Templeton, A. Estimates of lethal equivalents and the cost of inbreeding in mammals. Conserv. Biol. 2, 185–192 (1988).

    Article  Google Scholar 

  • 14.

    Hoeck, P. E. A., Wolak, M. E., Switzer, R. A., Kuehler, C. M. & Lieberman, A. A. Effects of inbreeding and parental incubation on captive breeding success in Hawaiian crows. Biol. Conserv. 184, 357–364 (2015).

    Article  Google Scholar 

  • 15.

    Jimenez, J. A., Hughes, K. A., Alaks, G., Graham, L. & Lacy, R. C. An experimental study of inbreeding depression in a natural habitat. Science (80-. ). 266, 271–273 (1994).

  • 16.

    Van Oosterhout, C., Zijlstra, W. G., Van Heuven, M. K. & Brakefield, P. M. Inbreeding depression and genetic load in laboratory metapopulations of the butterfly Bicyclus anynana. Evolution (N. Y). 54, 218–225 (2000).

  • 17.

    Szulkin, M., Garant, D., Mccleery, R. H. & Sheldon, B. C. Inbreeding depression along a life-history continuum in the great tit. J. Evol. Biol. 20, 1531–1543 (2007).

    CAS  PubMed  Article  Google Scholar 

  • 18.

    Wolak, M. E., Arcese, P., Keller, L. F., Nietlisbach, P. & Reid, J. M. Sex-specific additive genetic variances and correlations for fitness in a song sparrow (Melospiza melodia) population subject to natural immigration and inbreeding. Evolution (N. Y). 72, 2057–2075 (2018).

  • 19.

    Kennedy, E. S., Grueber, C. E., Duncan, R. P. & Jamieson, I. G. Severe inbreeding depression and no evidence of purging in an extremely inbred wild species-the chatham island black robin. Evolution (N. Y). 68, 987–995 (2014).

  • 20.

    Jamieson, I. G., Tracy, L. N., Fletcher, D. & Armstrong, D. P. Moderate inbreeding depression in a reintroduced population of North Island robins. Anim. Conserv. 10, 95–102 (2007).

    Article  Google Scholar 

  • 21.

    Norén, K., Godoy, E., Dalén, L., Meijer, T. & Angerbjörn, A. Inbreeding depression in a critically endangered carnivore. Mol. Ecol. https://doi.org/10.1111/mec.13674 (2016).

    Article  PubMed  Google Scholar 

  • 22.

    Sæther, B. E. & Bakke, Ø. Avian life history variation and contribution of demographic traits to the population growth rate. Ecology 81, 642–653 (2000).

    Article  Google Scholar 

  • 23.

    Beissinger, S. R. & McCullough, D. R. Population viability analysis. (University of Chicago Press, 2002).

  • 24.

    Lacy, R. C. Lessons from 30 years of population viability analysis of wildlife populations. Zoo Biol. 38, 67–77 (2019).

    PubMed  Article  Google Scholar 

  • 25.

    Traill, L. W., Bradshaw, C. J. A. & Brook, B. W. Minimum viable population size: A meta-analysis of 30 years of published estimates. Biol. Conserv. 139, 159–166 (2007).

    Article  Google Scholar 

  • 26.

    O’Grady, J. J. et al. Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biol. Conserv. 133, 42–51 (2006).

    Article  Google Scholar 

  • 27.

    Lacy, R. C., Miller, P. S. & Traylor-Holzer, K. Vortex 10 user’s manual. (2017).

  • 28.

    Ballou, J. D. & Lacy, R. C. in Population management for survival and recovery (eds. Ballou, J. D., Gilpin, M. & Foose, T. J.) 76–111 (Columbia University Press, 1995).

  • 29.

    Armbruster, P. & Reed, D. H. Inbreeding depression in benign and stressful environments. Heredity (Edinb). 95, 235–242 (2005).

    CAS  PubMed  Article  Google Scholar 

  • 30.

    Fox, C. W. & Reed, D. H. Inbreeding depression increases with environmental stress: an experimental study and meta-analysis. Evolution (N. Y). 65, 246–258 (2011).

  • 31.

    Baker, R. H. The avifauna of Micronesia, its origin, evolution and distribution. (University of Kansas Publications, 1951).

  • 32.

    Marshall, J. T. The endemic avifauna of Sapan, Tinian Guam and Palau. Condor 51, 200–221 (1949).

    Article  Google Scholar 

  • 33.

    Wiles, G. J., Bart, J., Beck, R. E. & Aguon, C. F. Impacts of the brown tree snake: patterns of decline and species persistence in Guam’s avifauna. Conserv. Biol. 17, 1350–1360 (2003).

    Article  Google Scholar 

  • 34.

    Savidge, J. A. Extinction of an island forest avifauna by an introduced snake. Ecology 68, 660–668 (1987).

    Article  Google Scholar 

  • 35.

    Haig, S. M., Ballou, J. D. & Casna, N. J. Genetic identification of kin in Micronesian kingfishers. J. Hered. 86, 423–431 (1995).

    Article  Google Scholar 

  • 36.

    Lacy, R. C., Ballou, J. D. & Pollak, J. P. PMx: Software package for demographic and genetic analysis and management of pedigreed populations. Methods Ecol. Evol. 3, 433–437 (2012).

    Article  Google Scholar 

  • 37.

    Ferrie, G. Using molecular genetic and demographic tools to improve management of ex situ avian populations. (University of Central Florida, 2017). http://stars.library.ucf.edu/etd/5709

  • 38.

    Zuur, A. F., Ieno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14 (2010).

    Article  Google Scholar 

  • 39.

    Burnham, K. . & Anderson, D. R. Model selection and multimodel inference: a practical information-theoretic approach. (Springer, 2002).

  • 40.

    Whittingham, M. J., Stephens, P. A., Bradbury, R. B. & Freckleton, R. P. Why do we still use stepwise modelling in ecology and behaviour?. J. Anim. Ecol. 75, 1182–1189 (2006).

    PubMed  Article  Google Scholar 

  • 41.

    Nietlisbach, P., Muff, S., Reid, J. M., Whitlock, M. C. & Keller, L. F. Nonequivalent lethal equivalents: Models and inbreeding metrics for unbiased estimation of inbreeding load. Evol. Appl. 12, 266–279 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 42.

    Zou, G. A modified poisson regression approach to prospective studies with binary data. Am. J. Epidemiol. 159, 702–706 (2004).

    PubMed  Article  Google Scholar 

  • 43.

    Bates, D., Mächler, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Article  Google Scholar 

  • 44.

    R Development Core Team. R: A language and environment for statistical computing. (2019).

  • 45.

    Lacy, R. C. & Pollak, J. P. Vortex: A stochastic simulation of the extinction process. (2017).

  • 46.

    Hemmings, N. L., Slate, J. & Birkhead, T. R. Inbreeding causes early death in a passerine bird. Nat. Commun. 3, 1–4 (2012).

    Article  CAS  Google Scholar 

  • 47.

    Tiira, K., Piironen, J. & Primmer, C. R. Evidence for reduced genetic variation in severely deformed juvenile salmonids. Can. J. Fish. Aquat. Sci. 63, 2700–2707 (2006).

    Article  Google Scholar 

  • 48.

    Wang, J., Hill, W. G., Charlesworth, D. & Charlesworth, B. Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rate. Genet. Res. 74, 165–178 (1999).

    CAS  PubMed  Article  Google Scholar 

  • 49.

    Husband, B. C. & Schemske, D. W. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution (N. Y). 50, 54–70 (1996).

  • 50.

    de Boer, R. A., Eens, M. & Müller, W. Sex-specific effects of inbreeding on reproductive senescence. Proc. R. Soc. B Biol. Sci. 285, (2018).

  • 51.

    Keller, L. F., Reid, J. M. & Arcese, P. Testing evolutionary models of senescence in a natural population: Age and inbreeding effects on fitness components in song sparrows. Proc. R. Soc. B Biol. Sci. 275, 597–604 (2008).

    CAS  Article  Google Scholar 

  • 52.

    Partridge, L. & Mangel, M. Messages from mortality: The evolution of death rates in the old. Trends Ecol. Evol. 14, 438–442 (1999).

    CAS  PubMed  Article  Google Scholar 

  • 53.

    Charlesworth, B. & Hughes, K. A. Age-specific inbreeding depression and components of genetic variance in relation to the evolution of senescence. Proc. Natl. Acad. Sci. U. S. A. 93, 6140–6145 (1996).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 54.

    Kristensen, T. N., Loeschcke, V. & Hoffmann, A. A. Linking inbreeding effects in captive populations with fitness in the wild: Release of replicated Drosophila melanogaster lines under different temperatures. Conserv. Biol. 22, 189–199 (2008).

    PubMed  Article  Google Scholar 

  • 55.

    Ryman, N. & Laikre, L. Effects of supportive breeding on the genetically effective population size. Conserv. Biol. 5, 325–329 (1991).

    Article  Google Scholar 

  • 56.

    Hedrick, P. W. & Garcia-Dorado, A. Understanding inbreeding depression, purging, and genetic rescue. Trends Ecol. Evol. 31, 940–952 (2016).

    PubMed  Article  Google Scholar 

  • 57.

    Kalinowski, S. T., Hedrick, P. W. & Miller, P. S. Inbreeding Depression in the Speke’s Gazelle Captive Breeding Program. Conserv. Biol. 14, 1375–1384 (2000).

    Article  Google Scholar 

  • 58.

    Gilligan, D. M. & Frankham, R. Dynamics of individual adaptation processes. Conserv. Genet. 4, 189–197 (2003).

    Article  Google Scholar 

  • 59.

    Christie, M. R., Marine, M. L., French, R. A. & Blouin, M. S. Genetic adaptation to captivity can occur in a single generation. Proc. Natl. Acad. Sci. U. S. A. 109, 238–242 (2012).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 60.

    Grueber, C. E., Waters, J. M. & Jamieson, I. G. The imprecision of heterozygosity-fitness correlations hinders the detection of inbreeding and inbreeding depression in a threatened species. Mol. Ecol. 20, 67–79 (2011).

    PubMed  Article  Google Scholar 

  • 61.

    Milligan, M. C., Wells, S. L. & McNew, L. B. A population viability analysis for sharp-tailed grouse to inform reintroductions. J. Fish Wildl. Manag. 9, 565–581 (2018).

    Article  Google Scholar 

  • 62.

    Research needs & implications for population management. Moßbrucker, A. M., Imron, M. A., Pudtatmoko, S., Pratje, P. & Sumardi. Modelling the fate of Sumatran elephants in Bukit Tigapuluh, Indonesia. J. For. Sci. 10, 5–18 (2016).

    Google Scholar 

  • 63.

    Sharpe, M. & Berggren, P. Indian Ocean humpback dolphin in the Menai Bay off the south coast of Zanzibar, East Africa is Critically Endangered. Aquat. Conserv. Mar. Freshw. Ecosyst. 29, 2133–2146 (2019).

    Article  Google Scholar 

  • 64.

    McQuillan, R. et al. Runs of homozygosity in European populations. Am. J. Hum. Genet. 83, 359–372 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 65.

    Caballero, A., Bravo, I. & Wang, J. Inbreeding load and purging: Implications for the short-term survival and the conservation management of small populations. Heredity (Edinb). 118, 177–185 (2017).

    CAS  PubMed  Article  Google Scholar 

  • 66.

    Liao, W. & Reed, D. H. Inbreeding-environment interactions increase extinction risk. Anim. Conserv. 12, 54–61 (2009).

    CAS  Article  Google Scholar 

  • 67.

    Melbourne, B. A. & Hastings, A. Extinction risk depends strongly on factors contributing to stochasticity. Nature 454, 100–103 (2008).

    ADS  CAS  PubMed  Article  Google Scholar 


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