The Evolution of Host-Plant Alternation in Aphids: Evidence for Specialization as a Dead End

The origins and maintenance of complex life cycles and of host associations are generally assumed by evolutionary ecologists to be governed by optimizing selection for maximal resource exploitation. Widely accepted hypotheses for the evolution of host-plant alternation (heteroecy) in aphids exemplify such assumptions. For example, the hypothesis of complementary host growth states that heteroecy is a result of selection for optimizing nutrient intake in a seasonally varying environment. However, these optimization hypotheses are inconsistent with many of the facts concerning aphid heteroecy. Heteroecy is frequent in aphids, and current knowledge of aphid phylogeny indicates that it originated several times. In contrast, heteroecy is rare or absent in other insects, implying that an adequate explanation must invoke features of aphids not found in other insect groups using similar resources. An alternative hypothesis, the fundatrix-specialization hypothesis, is based on the narrower range of tolerances of one of the seasonal morphs of the life cycle, the first spring female, or fundatrix. The fundatrix specializes on ancestral woody host plants when they are in their most favorable seasonal state. Heteroecy appears to be a consequence of the seasonal polymorphism of aphids, which causes some morphs (the fundatrices) to be more evolutionarily constrained than others (the summer females) in their abilities to acquire hosts. Some aphid lineages have escaped this constraint by replacing the ancestral fundatrix morph and remaining all year on former secondary hosts, thus becoming secondarily autoecious. Most of the large and species-rich groups of Aphidinae on herbaceous angiosperms probably are derived from ancestors showing such life-cycle reduction.