Reproductive Isolation Between Sympatric Races of Pea Aphids. I. Gene Flow Restriction and Habitat Choice

Determining the extent and causes of barriers to gene flow between genetically divergent populations or races of single species is an important complement to post facto analyses of the causes of reproductive isolation between recognized species. Sympatric populations of pea aphids (Acyrthosiphon pisum Harris, Homoptera: Aphididae) on alfalfa and red clover are highly genetically divergent and locally adapted. Here, hierarchical estimates of population structure based on Fst suggest that gene exchange between closely adjacent aphid populations on the two hosts is highly restricted relative to that among fields of the same host plant. Although these host-associated races are presently considered to be the same subspecies, they appear to be significantly reproductively isolated, suggesting incipient speciation. Habitat (host) choice was investigated as the first in a temporal series of factors that could reduce gene exchange between these sympatric populations. Field studies of winged colonists to newly planted fields of each host suggest pronounced habitat fidelity. This result was verified using replicated observations of the host choice behavior of different aphid genotypes for which the relative demographic performance on each host was known. These laboratory observations of behavior revealed a strong genetic correlation between habitat choice (or acceptance) and the relative performance in each habitat. Because mating occurs on the host plant, habitat choice in this system leads to assortative mating and is therefore a major cause of reproductive isolation between the sympatric pea aphid populations on alfalfa and clover. However, the extent of dispersal between hosts estimated from the field study of winged colonists (9–11%) is too great to be consistent with the genetic divergence estimated between the races. This suggests that barriers to gene flow other than host choice also exist, such as selection against migrants or hybrids in the parental environments, hybrid sterility, or hybrid breakdown.