Reproductive isolation between sympatric races of pea aphids. I. Gene flowrestriction and habitat choice

Determining the extent and causes of barriers to gene flow between genetica lly divergent populations or races of single species is an important comple ment to post facto analyses of the causes of reproductive isolation between recognized species. Sympatric populations of pea aphids (Acyrthosiphon pis um Harris, Homoptera: Aphididae) on alfalfa and red clover are highly genet ically divergent and locally adapted. Here, hierarchical estimates of popul ation structure based on F-st suggest that gene exchange between closely ad jacent aphid populations on the two hosts is highly restricted relative to that among fields of the same host plant. Although these host-associated ra ces are presently considered to be the same subspecies, they appear to be s ignificantly reproductively isolated, suggesting incipient speciation. Habi tat (host) choice was investigated as the first in a temporal series of fac tors that could reduce gene exchange between these sympatric populations. F ield studies of winged colonists to newly planted fields of each host sugge st pronounced habitat fidelity. This result was verified using replicated o bservations of the host choice behavior of different aphid genotypes for wh ich the relative demographic performance on each host was known. These labo ratory observations of behavior revealed a strong genetic correlation betwe en habitat choice (or acceptance) and the relative performance in each habi tat. 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 clove r. 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 ge netic divergence estimated between the races. This suggests that barriers t o gene flow other than host choice also exist, such as selection against mi grants or hybrids in the parental environments, hybrid sterility, or hybrid breakdown.