Antagonistic coevolution with parasites maintains host genetic diversity: an experimental test

Abstract

Genetic variation in natural populations is a prime prerequisite allowing populations to respond to selection, but is under constant threat from forces that tend to reduce it, such as genetic drift and many types of selection. Haldane emphasized the potential importance of parasites as a driving force of genetic diversity. His theory has been taken for granted ever since, but despite numerous studies showing correlations between genetic diversity and parasitism, Haldane's hypothesis has rarely been tested experimentally for unambiguous support. We experimentally staged antagonistic coevolution between the host Tribolium castaneum and its natural microsporidian parasite, Nosema whitei, to test for the relative importance of two separate evolutionary forces (drift and parasite-induced selection) on the maintenance of genetic variation. Our results demonstrate that coevolution with parasites indeed counteracts drift as coevolving populations had significantly higher levels of heterozygosity and allelic diversity. Genetic drift remained a strong force, strongly reducing genetic variation and increasing genetic differentiation in small populations. To our surprise, differentiation between the evolving populations was smaller when they coevolved with parasites, suggesting parallel balancing selection. Hence, our results experimentally vindicate Haldane's original hypothesis 60 years after its conception.

Figure 1.

Dynamics of allelic diversity during the selection experiment. (a) The average number of alleles (±s.e.m.). There was a strong effect of drift, as in small populations allelic number decreased over time, whereas numbers were equal in coevolved and control populations. For statistics, see table 1. (b) Shannon index of allelic diversity (±s.e.m.). Allelic diversity similarly showed strong effects of drift. Furthermore, allelic diversity was higher in coevolved than in control populations. For statistics, see table 2.

Figure 2.

Temporal dynamics of heterozygosity. (a) Observed heterozygosity (±s.e.m.) and (b) expected heterozygosity (±s.e.m.). Both indices of heterozygosity show qualitatively similar results (for statistics, see table 3), with drift reducing heterozygosity and coevolution maintaining heterozygosity.

Figure 3.

Trend of divergence during the selection experiment. (a) Pairwise F_ST (±s.e.m.) between all lines in an experimental block and analysed per generation. The graph shows the counteracting forces of overall host–parasite coevolution (i.e. keeping populations genetically similar) and genetic drift (small populations diverge faster). (b) Pairwise F_ST (±s.e.m.) between each of the evolved lines after 4, 8 or 12 generations and their respective replicate line immediately preceding time points. Coevolution seems to have no effect on the change in allelic composition over time, while populations that are experiencing stronger drift, diverge faster. Statistical details can be found in table 5.