Host-race formation and ecological speciation
A host plant, Cytisus scoparius
Speciation occurs when two populations of organisms accumulate sufficient differences that they are no longer able to interbreed. The differences may arise by chance when the two populations are physically separate. However, they may also occur because the two populations are experiencing different types of natural selection. The latter is now normally referred to as ecological speciation and is a major topic of current evolutionary research.
Plant-feeding insects provide excellent models for studying ecological speciation. Many species feed on more than one type of host plant where they may experience divergent selection to utilise the different types of food. Living on different host plants may also expose them to different risks of predation or parasitism which may again lead to dissimilar selection pressures. Plant-feeding insects often tend to mate on their host plant, and this assortative mating will reduce gene flow between different populations and increase the likelihood of adaptation to the different host plants.
Pea aphids feed on a broad range of host plants (though all in the pea family, Fabaceae) and have long been known to have host plant races. In a series of insightful studies Sara Via’s group (University of Maryland) showed that in the United States pea aphid populations have specialised on clover and alfalfa. Her group studied the genetics of host plant adaptation and identified a series of chromosomal regions associated with both host plant preference and performance.
The pea aphid was introduced to the New World and we were interested in exploring the extent to which pea aphid populations in the Old World were specialised on different host plants. To do this in a BBSRC-funded project led by Julia Ferrari we collected ~20 clones from each of 8 different host plant genera. We found that (with one exception discussed below) clones collected from one species tended to pick the same host plant species when given a choice of the range of eight plants (1). Moreover, the clones nearly always had higher survival and fecundity on their “home” plant species (2). The strength of the host-plant adaptation varied across populations, those from broom (Cytisus) and rest harrow (Ononis) being particularly specialised. We found several examples of clones that were well adapted to another species on the “wrong” host plant – we suspect these were vagrants.
The exception involved broad bean, Vicia faba. It is well known that nearly all pea aphid clones feed happily on broad bean. Clones collected on this host plant in the field are not particular specialised on this species, but instead seem to be members of other host plant races that have happened to colonise this “universal host”.
We recently published the final paper from this project, an analysis using molecular markers of the genetic structure of ~300 clones collected from the eight host plants in England and Germany. We found extensive genetic differentiation between pea aphids associated with different plant genera, although there was no evidence that this differentiation was correlated with the degree of divergence in host plant use (3).
It thus seems clear that the pea aphid has a very complex population structure with strong evidence for extensive host plant specialisation. What we don’t know is whether we are observing a stable situation or whether we are witnessing populations marching towards ecological speciation. Man has hugely altered the distribution of the pea aphid’s food plants since the invention of agriculture and perhaps we are observing the aphid’s evolutionary response. Alternatively the population structure may be stable with further specialisation and speciation being countered by gene flow mediated by aphids colonising the bridge host, Vicia faba. The new genetic resources that will become available when the pea aphid genome is published may provide tools to address this.
One issue we had been concerned with in our earlier work is whether the host plant an aphid was reared on might affect how its offspring faired on different hosts. Experiments with aphids reared on vetch (Lathyrus) and broad bean (Vicia faba) found no evidence for such maternal effects (4).
- Ferrari, J., Godfray, H.C.J., Faulconbridge, A.S., Prior, K. & Via, S. 2006 Population differentiation and genetic variation in host choice among pea aphids from eight host plant genera. Evolution 60, 1574-1584.
- Ferrari, J., Via, S. & Godfray, H.C.J. 2008 Population differentiation and genetic variation in performance on eight host plants in the pea aphid complex. Evolution 62, 2508-2524.
- Ferrari J., West J.A., Via S. & Godfray H.C.J. 2012 Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. Evolution 66(2), 375-390.
- McLean, A.H.C., Ferrari. J. & Godfray, H.C.J. 2009 Effects of the maternal and pre-adult host plant on adult performance and preference in the pea aphid, Acyrthosiphon pisum. Ecological Entomology 34, 330-338.