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Open Access Highly Accessed Research article

High variance in reproductive success generates a false signature of a genetic bottleneck in populations of constant size: a simulation study

Sean M Hoban12, Massimo Mezzavilla3, Oscar E Gaggiotti4, Andrea Benazzo1, Cock van Oosterhout5 and Giorgio Bertorelle1*

Author Affiliations

1 Department of Life Sciences and Biotechnology, University of Ferrara, via Borsari 46, Ferrara I-44121, Italy

2 National Institute for Mathematical and Biological Synthesis (NIMBios), The University of Tennessee, Knoxville, TN 37996, USA

3 Institute for Maternal and Child Health, IRCCS, University of Trieste, via dell’Istrai 65, Trieste I-34137, Italy

4 School of Biology, Scottish Oceans Institute, University of St Andrews, St Andrews, Fife KY16 8LB, UK

5 School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK

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BMC Bioinformatics 2013, 14:309  doi:10.1186/1471-2105-14-309

Published: 16 October 2013

Abstract

Background

Demographic bottlenecks can severely reduce the genetic variation of a population or a species. Establishing whether low genetic variation is caused by a bottleneck or a constantly low effective number of individuals is important to understand a species’ ecology and evolution, and it has implications for conservation management. Recent studies have evaluated the power of several statistical methods developed to identify bottlenecks. However, the false positive rate, i.e. the rate with which a bottleneck signal is misidentified in demographically stable populations, has received little attention. We analyse this type of error (type I) in forward computer simulations of stable populations having greater than Poisson variance in reproductive success (i.e., variance in family sizes). The assumption of Poisson variance underlies bottleneck tests, yet it is commonly violated in species with high fecundity.

Results

With large variance in reproductive success (Vk ≥ 40, corresponding to a ratio between effective and census size smaller than 0.1), tests based on allele frequencies, allelic sizes, and DNA sequence polymorphisms (heterozygosity excess, M-ratio, and Tajima’s D test) tend to show erroneous signals of a bottleneck. Similarly, strong evidence of population decline is erroneously detected when ancestral and current population sizes are estimated with the model based method MSVAR.

Conclusions

Our results suggest caution when interpreting the results of bottleneck tests in species showing high variance in reproductive success. Particularly in species with high fecundity, computer simulations are recommended to confirm the occurrence of a population bottleneck.

Keywords:
Conservation; Heterozygosity excess; M-ratio; MSVAR; FPR; Sweepstakes reproduction; Type I error; Variance in reproductive success