Consequences of inbreeding and reduced genetic variation on tolerance to cadmium stress in the midge Chironomus riparius
Introduction
When populations decrease in size, genetic drift can lead to reduced levels of genetic variation. This loss of variation has been shown to enhance extinction risk of populations in the long term due to loss of evolutionary potential which enables populations to adapt to changing environmental conditions (Frankham et al., 2004). Additionally, small populations may suffer from inbreeding due to increased levels of homozygosity of deleterious alleles, which frequently results in the loss of fitness (Charlesworth and Charlesworth, 1987). This process, termed inbreeding depression, has been documented to affect both natural and caged organisms subjected to severe population bottlenecks (Armbruster et al., 2000). In summary, loss of genetic variation and increased genome-wide homozygosity are likely to accelerate extinction processes in plants and animals (Charlesworth and Charlesworth, 1987, Saccheri et al., 1998, Reed et al., 2003).
Furthermore, empirical studies showed that inbreeding depression can be reinforced under stressful environmental conditions, like chemical exposure (summarized in Armbruster and Reed, 2005). For instance, Kristensen et al. (2003) showed that only under environmental stress highly inbred Drosophila buzzatii strains produce significantly less progeny than outbred individuals. These findings might have severe implications for both conservation strategies in polluted environments as well as for toxicological exposure assays, for populations of endangered species as well as caged laboratory test strains show reduced levels of genetic variability (Norris et al., 2001, Joron and Brakefield, 2003, Frankham et al., 2004). Furthermore, inbreeding is unavoidable in small populations (Bijlsma et al., 2000). Therefore, it is of high ecotoxicological importance to investigate interactions between inbreeding and chemical stress. These studies will allow us to assess the consequences of environmental stress on the fitness of natural populations.
To test if inbreeding and the level of genetic variation influence tolerance to chemical exposure, we generated nine laboratory strains of the non-biting midge Chironomus riparius (Diptera: Chironomidae) which differed in their level of inbreeding (inbreeding coefficient F = 0, 0.125 and 0.375). The level of genetic variation within the strains was verified using microsatellite analysis (Nowak et al., 2006). All strains were exposed to a gradient of sediment-associated Cd and various life-history traits, including reproduction parameters, were recorded.
The main questions of this study were:
- (i)
Does inbreeding affect life-history traits of C. riparius strains in the laboratory?
- (ii)
Does inbreeding and reduced genetic variation affect susceptibility of C. riparius to Cd stress?
- (iii)
Are ‘validity criteria’, like thresholds for control mortality, sufficient to prevent test results from bias due to inbreeding effects?
The results of this study are discussed with special emphasis for their consequences on both ecotoxicological test bioassays and species conservation strategies.
Section snippets
Inbreeding procedure and culture conditions
We established nine independent C. riparius strains from a laboratory culture which has been reared in our laboratory for 3 years. In order to obtain a high level of genetic variation, this culture had been established from a crossbred of 11 laboratory strains from seven different countries (Nowak et al., 2007). The nine strains were generated using different numbers of egg ropes for the founder generation. Three independent highly inbred strains (high In) were established performing two
Residual analysis of sediment and water
At the end of the life-cycle experiments, mean percentages of measured Cd concentrations in the sediment ranged from 60% (1.2 mg Cd/kg dw) to 74% (0.9 mg Cd/kg dw) of nominals. Cd concentrations in the water samples varied between 3.87 μg/L (0.6 mg Cd/kg dw) and 9.55 μg/L (0.3 mg Cd/kg dw, Table 1).
Genetic analyses
Measuring of allelic variation at five microsatellite loci led to observed heterozygosity levels ranging from 0.17 (high In III) to 0.41 (Out III). Generally, both observed and expected heterozygosity, the
Discussion
To our knowledge, we present the first study which investigates the combined effects of inbreeding, reduced heterozygosity and chemical stress with an ecotoxicological model species under standardized conditions. Recovery rates of Cd in the experiments were similar among replicates and treatments. Thus, observed variation in life-history response between C. riparius strains cannot be explained by variations in sediment contamination between the tests. Because earliest larval stages have been
Acknowledgements
We thank Agnes Sieratowicz and Simone Galluba for their kind help in test accomplishment and Maren Heß for expert technical assistance. Markus Pfenninger gave valuable hints concerning the experimental design. This project was financially supported by the ‘Baden-Württemberg Programm Lebensgrundlage Umwelt und ihre Sicherung’ (BWPLUS, BWR 22018).
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These authors equally contributed to the manuscript.