1 Zoological Museum, University of Zürich (Switzerland), 2 Department of Ecology, Ethology and Evolution, University of Illinois, Urbana (USA), 3 Zoological Institute, University of Zürich (Switzerland)
Whether the high amount of allelic polymorphism at protein-coding loci observed in natural populations of many organisms is selectively neutral or adaptive has been disputed since the data became available. The assumption of neutrality is widely used for population genetic, phylogenetic and ecogenetic analyses based on protein electrophoretic markers. Recent studies have repeatedly questioned the generality of the neutrality assumption. We report significant differences among genotypes of an enzyme locus in anuran larval performance traits closely related to individual fitness. At the locus lactate dehydrogenase-B (LDH-B) the European water frog Rana lessonae is highly polymorphic for two alleles (b,e) through most of its range. We tested larval performance in an artificial pond experiment where tadpoles of Rana lessonae from northern Switzerland and of the hybrid Rana esculenta (Rana ridibunda x Rana lessonae) were reared together. Duration of larval period and size at metamorphosis each differed significantly between the two homozygous LDH-B genotypes of Rana lessonae. Homozygotes for one of the two common alleles (e) had a shorter larval period, and reached greater mass at metamorphosis than b/b homozygotes; b/e heterozygotes had intermediate values for both traits. That e/e homozygotes performed better than b/b homozygotes in both traits is interesting because time to metamorphosis and size at metamorphosis in anuran tadpoles are usually viewed as alternative life history modes reflecting a tradeoff between (1) starting post-metamorphic life at a large size, and (2) avoiding larval death caused by drying-up of ephemeral ponds. The Rana lessonae parents used in this experiment came from a single pond; because degree of linkage disequilibrium in this population (for example reflecting a recent bottleneck) is unknown, it cannot be excluded that the differential larval performance is caused by an anonymous tightly linked gene rather than by the LDH-B locus itself. A causal involvement of LDH-B appears nevertheless plausible, since this enzyme takes part in the central energy-metabolizing processes, and fitness differences among genotypes of protein loci reported for other organismal groups have among others included LDH-B. Whether balancing selection, the alternate common allele (b) or the heterozygous genotype being superior in other life stages or under other environmental conditions, is responsible for the broad maintenance of LDH-B polymorphism in Rana lessonae, remains to be tested.