Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers Lukas F. Keller 1* , Kathryn J. Je¡ery 2 { Peter Arcese 3 , Mark A. Beaumont 2 {, Wesley M. Hochachka 4 , James N. M. Smith 5 and Michael W. Bruford 2 { 1 Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA 2 Conservation Genetics Group, Institute of Zoology, Regent’s Park, London NW1 4RY, UK 3 Centre for Applied Conservation Biology, Forest Sciences, 2424 Main Mall, University of British Columbia,Vancouver, B.C., Canada,V6T 1Z4 4 Cornell Laboratory of Ornithology, 159 Sapsucker Woods Road, Ithaca, NY 14850, USA 5 Centre for Biodiversity Research and Department of Zoology, University of British Columbia,Vancouver, B.C., Canada,V6T1Z4 Population bottlenecks are often invoked to explain low levels of genetic variation in natural populations, yet few studies have documented the direct genetic consequences of known bottlenecks in the wild. Empirical studies of natural population bottlenecks are therefore needed, because key assumptions of theoretical and laboratory studies of bottlenecks may not hold in the wild. Here we present microsatellite data from a severe bottleneck (95% mortality) in an insular population of song sparrows ( Melospiza melodia). The major ¢ndings of our study are as follows: (i) The bottleneck reduced heterozygosity and allelic diversity nearly to neutral expectations, despite non-random survival of birds with respect to inbreeding and wing length. (ii) All measures of genetic diversity regained pre-bottleneck levels within two to three years of the crash. This rapid recovery was due to low levels of immigration. (iii) The rapid recovery occurred despite a coincident, strong increase in average inbreeding. These results show that immigration at levels that are hard to measure in most ¢eld studies can lead to qualitatively very di¡erent genetic outcomes from those expected from mutations only. We suggest that future theoretical and empirical work on bottlenecks and metapopulations should address the impact of immigration. Keywords: bottleneck; genetic variation; immigration; inbreeding; microsatellites 1. INTRODUCTION Genetic diversity in populations and the evolutionary forces that a¡ect it are central to both evolutionary (e.g. Wright 1931; Haldane 1932; Fisher 1958) and conservation biology (e.g. O’Brien et al. 1985; Lande 1988; Frankham 1995). When populations undergo temporary, large reduc- tions in sizeöso-called population bottlenecks (Wright 1931; Nei et al. 1975)öthey lose genetic diversity through random drift. Bottlenecks are therefore thought to be involved in speciation events (e.g. Mayr 1963; Carson 1990; Slatkin 1996), heterozygote de¢ciency in natural populations (Nei & Graur 1984), low levels of genetic variation (Bonnell & Selander 1974; O’Brien et al. 1983; Ellegren et al. 1996; Groombridge et al. 2000), and reduced reproductive function (Wildt et al. 1987; Madsen et al. 1999). Following Nei et al. (1975) a number of theoretical (e.g. Maruyama & Fuerst 1984; Watterson 1984; Maruyama & Fuerst 1985a,b ; Lacy 1987) and laboratory studies (e.g. Bryant et al. 1981; McCommas & Bryant 1990; Leberg 1992; Richards & Leberg 1996; Saccheri et al. 1999) have addressed the genetic e¡ects of bottlenecks. However, while genetic data have often been used to infer the occurrence of bottlenecks in natural populations (e.g. Menotti-Raymond & O’Brien 1993; Hoelzel et al. 1993; Ross et al. 1993; Taylor et al. 1994; Dorit et al. 1995; Cornuet & Luikart 1996; Houlden et al. 1996; Vincek et al. 1997), few studies have actually documented the genetic consequences of known bottlenecks in natural populations (Gallardo et al. 1995; Brookes et al. 1997; Bouzat et al. 1998; Glenn et al. 1999). The genetic outcome of bottle- necks in nature may di¡er from those in experimental settings because some key assumptions made in those studies may not hold in the wild (Carson 1990) and because the ecological context of bottlenecks is di¡erent in the wild. For example, in laboratory studies individuals are removed at random to simulate a bottleneck. In the wild, however, individuals may not die at random and selection may be strong (Bancroft et al. 1995a,b). More- over, most theoretical and laboratory studies of bottle- necks have assumed a single, completely isolated population. Many natural populations, however, are part of a set of connected populations and exchange genes with other populations. Thus, data from natural popula- tions with known bottleneck histories, including data on the individuals that survived the bottleneck, are needed to establish the degree to which laboratory and theoretical results re£ect bottleneck e¡ects in nature (Ardern et al. 1997; Amos & Harwood 1998). Proc. R. Soc. Lond. B (2001) 268, 1387^1394 1387 © 2001 The Royal Society Received 29 September 2000 Accepted 2 February 2001 doi 10.1098/rspb.2001.1607 * Author and address for correspondence: Division of Environmental and Evolutionary Biology, Institute of Biomedical and Life Sciences, Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ , UK (l.keller@bio.gla.ac.uk). {Present address: Cardi¡ School of Biosciences, Cardi¡ University, Cardi¡ CF1 3TL, UK. {Present address: School of Animal and Microbial Sciences, University of Reading,Whiteknights, PO Box 228, Reading RG6 6AJ, UK. on March 21, 2016 http://rspb.royalsocietypublishing.org/ Downloaded from