On the neutrality of molecular genetic markers: pedigree analysis of genetic variation in fragmented populations

• Published in: Molecular ecology Vol. 13; no. 5; pp. 1025 - 1034
• Main Authors: Oosterhout, V. van, Heuven, M.K. van, Brakefield, P.M
• Format: Journal Article
• Language: English
• Published: Oxford, UK Blackwell Science Ltd 01.05.2004
• Subjects: alleles; allozymes; Animals; associative overdominance; background selection; Bicyclus anynana; Butterflies - genetics; Computer Simulation; Evolution, Molecular; Genetic Drift; genetic markers; Genetic Markers - genetics; Genetic Variation; Genetics, Population; heterozygosity; Isoenzymes; linkage disequilibrium; Linkage Disequilibrium - genetics; metapopulation; Models, Genetic; mutation; natural selection; Nymphalidae; Pedigree; Selection, Genetic; temporal genetic analysis
• ISSN: 0962-1083; 1365-294X
• DOI: 10.1111/j.1365-294X.2004.02114.x

Many studies employ molecular markers to infer ecological and evolutionary processes, assuming that variation found at genetic loci offers a reliable representation of stochastic events in natural populations. Increasingly, evidence emerges that molecular markers might not always be selectively neutral. However, only a few studies have analysed how deviations from neutrality could affect estimates of genetic variation, using populations with known genealogy. We monitored changes in allozyme variation over eight generations in captive metapopulations of the butterfly Bicyclus anynana. Population demography was recorded by individually marking 35 000 butterflies and constructing pedigrees. We designed a computer program that simulated the inheritance of founder allozyme alleles in butterfly pedigrees. We thus tested whether the observed transmission of allozyme alleles could be explained by random genetic drift alone, or whether there was evidence for positive or negative selection. This analysis showed that in the smallest metapopulations the loss of allozyme variation exceeded the neutral rate. Possibly, linkage disequilibria between deleterious mutations and marker alleles resulted in background selection and a faster erosion of allozyme variation. In larger metapopulations, one locus (MDH) showed a significant heterozygote excess and smaller than expected loss in heterozygosity, observations consistent with (associative) overdominance. This study demonstrates that the neutrality of molecular markers cannot always be assumed, particularly in small populations with a high mutation load.