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Effects of Seed Bank Disturbance on the Fine-Scale Genetic Structure Of Heredity (2003) 91, 475–480 & 2003 Nature Publishing Group All rights reserved 0018-067X/03 $25.00 www.nature.com/hdy Effects of seed bank disturbance on the fine-scale genetic structure of populations of the rare shrub Grevillea macleayana PR England1, RJ Whelan and DJ Ayre Institute for Conservation Biology, Department of Biological Sciences, University of Wollongong, NSW 2522, Australia Dispersal in most plants is mediated by the movement of structure with two sites that had been strongly affected by seeds and pollen, which move genes across the landscape road building using a test for spatial autocorrelation of differently. Grevillea macleayana is a rare, fire-dependent genotypes. High selfing levels inferred from genotypes at all Australian shrub with large seeds lacking adaptations for four sites implies that pollen dispersal is limited. Consistent dispersal; yet it produces inflorescences adapted to pollina- with this, we observed substantial spatial clustering of genes tion by highly mobile vertebrates (eg birds). Interpreting fine- at 10 m or less in the two undisturbed populations and argue scale genetic structure in the light of these two processes is that this reflects the predicted effects of both high selfing confounded by the recent imposition of anthropogenic dis- levels and limited seed dispersal. In contrast, at the two sites turbances with potentially contrasting genetic consequences: disturbed by road building, spatial autocorrelation was weak. (1) the unusual foraging behaviour of exotic honeybees This suggests there has been mixing of the seed bank, and 2. widespread disturbance of the soil-stored seedbank counteracting the naturally low dispersal and elevated selfing by road building and quarrying. To test for evidence of fine- due to honeybees. Pollination between near neighbours with scale genetic structure within G. macleayana populations reduced relatedness potentially has fitness consequences and to test the prediction that such structure might be for G. macleayana in disturbed sites. masked by disturbance of the seed bank, we sampled two Heredity (2003) 91, 475–480. doi:10.1038/sj.hdy.6800308 sites in undisturbed habitat and compared their genetic Keywords: spatial autocorrelation; microsatellites; disturbance; seed dispersal Introduction kart and England, 1999). Research is revealing that many systems exhibit structure at fine scales, but a detailed Characterising gene flow and structure at the finest scale understanding of the biology of a species is often within populations is critical to understanding how required to interpret the observed patterns with respect broader scale genetic patterns are generated. Fine-scale to the relative importance of short- and long-range structure promotes the generation of novel genotypes dispersal mechanisms. locally, promoting evolution (Wright, 1969). Fine-scale In plants, a combination of limited dispersal of seed structure and habitat patch size and shape can interact to and pollen has long been predicted to generate fine-scale affect the rate of accumulation of deleterious mutations genetic structuring (see simulations of Turner et al, 1982). (Kawata, 2001). It is also important to identify when However, empirical findings do not always match these intrapopulation structure exists because this can predictions and theoretical work suggests that spatial compromise the validity of population genetic analyses autocorrelation should be lower than generally expected that assume homogeneity, such as estimates of gene (Epperson, 1995). High levels of pollen flow and seed frequencies, heterozygosity, Hardy–Weinberg propor- dispersal result in no detectable spatial genetic structure tions and outcrossing rates. Sampling strategies designed in lodgepole pine (Epperson and Allard, 1989) and, in to measure these parameters and to conserve genetic Camellia japonica, the effects of low seed dispersal appear biodiversity also require the delineation of fine-scale to have been ameliorated by overlapping seed shadows genetic structure. and high levels of pollen flow (Ueno et al, 2000). In There is a burgeoning of interest in the study of gene contrast, Smouse et al (2001) found surprisingly small flow at local scales that is being fueled by recent effective pollen dispersal neighbourhoods in Quercus alba, advances in genetic and statistical methodologies (Lui- which has been assumed to have widely dispersing pollen. Bonnin et al (2001) demonstrated substantial fine- scale structure in the highly selfing Medicago truncatula. Correspondence: PR England, Institute for Conservation Biology, Grevillea macleayana (family Proteaceae) is a rare shrub Department of Biological Sciences, University of Wollongong, NSW (Briggs and Leigh, 1996) that has a restricted and 2522, Australia. E-mail: [email protected] 1Current address: Laboratoire d’Ecologie Alpine, Universite´ Joseph fragmented distribution in south-eastern New South Fourier, BP 53-38041, Grenoble cedex 9, France. Wales (McGillivray, 1993; Makinson, 1999). It has been Received 3 April 2002; accepted 4 April 2003 the focus of numerous ecological and genetic studies Spatial genetic structure in G. macleayana PR England et al 476 (reviewed in Whelan et al, 2000). The species is pollinated index with 95% confidence intervals generated by boot- by a range of bird species and introduced honeybees strapping across loci (Table 1). See England et al (2002) (Apis mellifera), it is fully self-compatible, capable of seed for a more extensive population genetic analysis of these set by autogamy (Vaughton, 1995) and outcrossing rates and other populations. Plants from two populations, appear to vary dramatically among populations (Ayre Wright’s Beach and Long Beach South, were sampled et al, 1994; England et al, 2001). Although plants are killed from along the edges of roads that had been constructed by fire, populations persist by recruitment from a soil- with heavy machinery. At Wright’s Beach we sampled 20 stored seed bank, following breaking of dormancy by fire plants bordering approximately 200 m of a more ex- or soil disturbance (Edwards and Whelan, 1995). Seeds tensive population that extends several hundred metres have no obvious adaptations that would facilitate seed further along the road. We sampled 28 plants at Long dispersal. Beach South, comprising what appears to be the entire Like many species in the family Proteaceae, G. population in that locality. The roads at both sites were macleayana shows obvious adaptations for bird pollina- sloping and lined with earth mounds indicative of tion (Makinson, 1999). Its numerous inflorescences are substantial soil disturbance. In many cases, plants were large, colourful and nectar-laden. Its pollinators are growing directly in the earth mounds or in drainage abundant and active (Vaughton, 1996) suggesting that ditches. We have called these disturbed sites. The other pollen-mediated dispersal is important. However, several two sites were in what appears to be relatively factors potentially limit the contribution of bird-mediated undisturbed habitat, although foot tracks exist in both pollen movement to gene flow in G. macleayana. (1) sites and a sealed road borders the Hyam’s Beach site The species is self-compatible and high contemporary (Figure 1). The Abraham’s Bosom site, where we selfing levels have been recorded in some populations sampled all 31 mature plants, is in a flat open heathland (Ayre et al, 1994; England et al, 2001, 2002). (2) Seeds with some low Eucalypt trees. The Hyam’s Beach site is show no obvious adaptations for dispersal, instead mostly in flat, low woodland with a dense understory. lodging in soil (and presumably germinating) close to We sampled 23 plants at this site. Later investigation the mother plant (Edwards and Whelan, 1995). (3) revealed that the population at this locality is substan- Introduced honeybees appear to be disrupting pollina- tially larger. We have called these ‘‘undisturbed sites’’, tion patterns by interfering with the role vertebrates may and we assume that they are closer to what may be have formerly played as the primary pollen vector described as the natural state. (England et al, 2001, 2002). We used the spatial autocorrelation method of Smouse G. macleayana is an obligate seeder and populations and Peakall (1999), as implemented in the software naturally depend on fire to regenerate from the seed package GenAlEx (Peakall and Smouse, 2001), to gen- bank (Edwards and Whelan, 1995). Although erate autocorrelelograms with 5 m size classes for each G. macleayana has no obvious natural means of seed population out to a maximum distance of 50 m. Beyond dispersal, its germination is readily triggered by habitat 50 m all populations began to exhibit empty size classes. disturbance/soil movements presumably via seed coat We reasoned that 5 m was the maximum viable resolu- scarification (Edwards and Whelan, 1995) and a sub- tion because many plants had diameters approaching stantial proportion of extant populations occur along but not exceeding this size. Untransformed Euclidean roads and in gravel quarries. We postulated that soil distances were used. disturbance may therefore promote genetic mixing Tests for statistical significance in GenAlEx were within affected populations. Natural patterns of fine- performed by random permutation. This consists of scale structure are sensitive to anthropogenic distur- randomly shuffling the individual genotypes among the bances associated with the exploitation of natural areas, geographic locations and recomputing autocorrelation
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