A polymorphism maintained by opposite patterns of parasitism and predation

Abstract

Although polymorphism is a widespread phenomenon that has been recognized for nearly two centuries, the basic mechanisms maintaining most polymorphisms in nature are unknown. We present evidence that a polymorphism can be maintained exclusively by balanced selection from two predatory species. For field and laboratory experiments, we used the pea aphid, Acyrthosiphon pisum, which occurs as 'green' and 'red' colour morphs, and two species that attack pea aphids, the parasitoid Aphidius ervi and the predator Coccinella septempunctata. We found that when parasitism rates in the field were high relative to predation rates, the proportion of red morphs increased relative to green morphs, whereas the converse was true when predation rates were high relative to parasitism rates. Detailed laboratory and field studies confirmed that green morphs suffer higher rates of parasitism than red morphs, whereas red morphs are more likely to be preyed on by predators than green morphs are. We present a mathematical model that demonstrates that biased density-dependent parasitism and/or predation on different morphs is sufficient to maintain the colour polymorphism in the population. Our findings support an important role for predation in the maintenance of genetic diversity.