Genetic erosion, inbreeding and reduced fitness in fragmented populations of the endangered tetraploid pea Swainsona recta

Abstract

Genetic variation and fixation coefficients were measured for 17 fragmented populations of the endangered tetraploid pea Swainsona recta ranging in size from 1 to 430 flowering plants. Allelic richness and fixation coefficient were correlated with the log population size, suggesting that reduced population size is accompanied by genetic erosion, primarily due to a loss of rare (q<0.1) alleles, and increased inbreeding. Comparative germination and growth studies of seed from five populations representing three different levels of inbreeding (low F=0.34, medium F=0.43, high F=0.57) showed a significant reduction in percentage seed germination at 2 weeks in the single high F treatment population. There were no effects on survivorship and growth beyond this up until 141 days. Results suggest that polyploidy has not prevented erosion of genetic variation at the population level, as has previously been suggested. However, the production of partial heterozygotes, e.g. AABC and AAAB, under inbreeding may be mitigating inbreeding depression assuming a partial dominance model of gene expression. Conservation effort should concentrate on populations larger than 50 sexually reproductive plants, as these appear capable of maintaining high genetic diversity and exhibit no immediate evidence of inbreeding depression, despite some elevation of the fixation coefficient.

Introduction

In Australia, as in many parts of the world, habitat destruction and fragmentation has been an increasingly dominant process shaping landscapes over the last 100–150 years. For species that are now restricted to such fragmented habitats determining the viability of small, isolated, remnant populations is a research priority if informed management decisions are to be made. Until recently, conservation strategies for endangered species were aimed primarily at preserving the existence of the individual and its habitat. Such actions are crucial to stabilise species in the short-term. More recently however, interest has focused on the genetic effects of population reduction, including genetic erosion and inbreeding, and the implications for individual fitness, population viability and regional species persistence (Barrett and Kohn, 1991, Ledig, 1992, Young, Boyle and Brown, 1996).

Population genetic theory predicts that small, isolated populations will lose genetic diversity and become increasingly differentiated due to founder effects, increased random genetic drift, and reduced inter-population gene flow, while increased inbreeding may lower individual heterozygosity. Such effects have serious implications for population persistence and the probability of species extinction. In the short-term a loss of heterozygosity can lower individual fitness, while erosion of variation at loci controlling self-incompatibility may reduce mate availability, as has been recently demonstrated for the Lakeside Daisy (Hymenoxys acaulis var. glabra) (DeMauro, 1993). In the longer term, reductions in genetic variation may affect a species' ability to adapt to changing selection pressures thus limiting future evolutionary potential.

Empirical studies using allozyme markers have shown significant positive relationships between population size and genetic variation for a number of plant species, e.g. McClenaghan and Beauchamp, 1986, Sampson, Hopper and James, 1988. More recently, similar relationships have been observed for species which have been made rare due to habitat loss, e.g. van Treuren, Bijlsma, van Delden and Ouborg, 1991, Prober & Brown, 1994, Raijmann et al, 1994, Prober, Spindler & Brown, 1999, Young, Brown and Zich, 1999. Similarly, effects of reduced population size on levels of self-fertilisation (Raijmann et al., 1994) and patterns of paternity (Young and Brown, 1999) have been identified. However, it has also become clear that genetic responses to reduced size and increased population isolation are likely to be species-specific, depending on life history characteristics such as breeding system, dispersal syndrome and longevity (Young et al., 1996).

One factor with clear potential to delimit genetic changes in small isolated populations, and their effects on population persistence, is ploidy level. For example theory suggests that, for a given population size, autotetraploids are less subject to loss of allelic richness by genetic drift than diploids (Bever and Felber, 1992). Similarly, inbreeding is expected to erode heterozygosity more slowly in autotetraploids than in diploids (Glendinning, 1989) and, under partial dominance, less inbreeding depression is expected due to the existence of partial heterozygotes (Husband and Schemske, 1997). Thus polyploid species may be less subject to negative genetic effects of low population size than their diploid counterparts.

In this study genetic diversity, levels of inbreeding and plant fitness were assessed in remnant populations of the putative tetraploid pea Swainsona recta Lee (Fabaceae), a species which has been subject to severe habitat loss due to destruction and fragmentation of its grassland habitat. Specifically the study examines whether small isolated populations of S. recta have lower genetic diversity, higher rates of inbreeding and lower individual fitness than large populations. The intention was to determine population size thresholds beyond which such genetic effects are unlikely to adversely effect viability so that these populations could be given priority for conservation.