Decision making by generalist and specialist aphids with the same genotype
Introduction
Among the myriad factors that could account for the high incidence of plant specialisation in phytophagous insects (Fiedler, 1998, Uero et al., 1999, Crespi and Sandoval, 2000, Dicke, 2000, Gange et al., 2002, Janz and Thompson, 2002, Oppenheim and Gould, 2002) is the fact that their nervous systems are simple and may be unable to efficiently recognise multiple host-plant species. This ‘neural limitations’ hypothesis (Bernays and Funk, 1999, Bernays, 2001) has received some support from experimental studies. Generalist whiteflies (Bemisia tabaci) and grasshoppers (Schistocerca americana) show disturbed foraging behaviour when presented with mixtures of host plants (Bernays, 1999, Bernays and Bright, 2001). The monophagous butterflies Polygonia satyrus, Vanessa indica and Inachis io are better able to discriminate poor from good-quality nettles for egg laying relative to the generalists P. c-album and Cynthia cardui (Janz and Nylin, 1997), and a generalist population of P. c-album will oviposit more often on a Lamium non-host than a specialist population (Nylin et al., 2000). Specialised populations of the aphid Uroleucon ambrosiae from the eastern US initiate phloem feeding faster on Ambrosia trifida than generalist south-western populations and remain in the phloem for a longer period over 12 h (Bernays and Funk, 1999).
As indicated above, a common experimental procedure within studies of neural limitations is to analyse the feeding behaviour of populations or closely-related species with differing host-plant ranges. This is potentially problematic because it is unlikely that the only genes differentially expressed between these populations or species are related to host-plant range.
Along with some other host-alternating aphid species, the study organism of this paper, the black bean aphid, Aphis fabae, is remarkable in that it can exist as generalist and specialist forms within the life cycle of a single clone (genotype). Eggs hatch in spring and after several parthenogenetic, viviparous generations on the primary (‘winter’) host plant, the spindle tree, E. europaeus, winged forms are produced that migrate to herbaceous secondary (‘summer’) hosts. During the summer months both wingless and winged parthenogenetic, viviparous virginoparae exist, the latter being induced in response to increases in aphid density and changes in food quality. Both forms are highly polyphagous. In the short days of autumn special winged parthenogenetic females (the gynoparae) are produced immediately prior to the production of winged males. The gynoparae, which are almost identical morphologically to the summer winged virginoparae (Hardie, 1980), and males fly to a single overwintering host-plant species (E. europaeus) where gynoparae give birth to sexual females, which mate with males and lay eggs. Summer winged virginoparae and gynoparae from the same clone are therefore genetically identical, extremely similar morphologically, both parthenogenetic and both viviparous, yet differ dramatically in host-plant range. This system appears to approach the experimental ideal of an isolated biological trait: host-plant range.
In this paper the efficiency of decision making of the gynopara on its host plant E. europaeus is analysed relative to that of the generalist summer winged virginopara (hereafter ‘winged virginopara’) on four of its herbaceous hosts: Beta vulgaris (‘beet’), Papaver dubium (‘poppy’), Rumex obtusifolius (‘dock’) and Vicia faba (‘bean’). Euonymus europaeus is also accepted as a host plant by the winged virginopara in the laboratory (Kennedy and Booth, 1951, Powell and Hardie, 2000, Powell and Hardie, 2001) and the behaviour of both forms is compared on this host. Additionally, analyses of behaviour over the first few minutes of plant contact on three mutual non-hosts, Euonymus alatus (‘winged spindle’), Prunus padus (‘bird cherry’) and Brassica pekinensis (‘Chinese cabbage’) are carried out to determine the relative efficiency of plant rejection behaviour.
Aphids are phloem feeders and probe the plant tissue with long hollow stylets. Typically on a suitable host plant they make an initial probe which may or may not arrest the aphid (Powell and Hardie, 2000, Tosh et al., 2002) and lead to longer tissue probes. During prolonged penetrations the mouthparts pass through the tissue extracellularly (Tjallingii and Hogen Esch, 1993), occasionally puncturing (probably sampling: Powell et al., 1995, Martin et al., 1997) neighbouring cells. After one or several entries into the phloem vessels, stylet penetration of a suitable host may result in sustained phloem ingestion. First parturition often occurs before significant ingestion from the phloem vessels and is probably initiated in response to cues in the peripheral tissues (Tosh et al., 2002). Here we analyse the speed and accuracy of key decisions during the whole of this host-plant utilisation process, from initial probing, through parturition to entry and acceptance of the phloem vessels, using a combination of non-invasive video monitoring and electrical monitoring of stylet behaviour (the electrical penetration graph, EPG).
Section snippets
Insects and plants
The clone of Aphis fabae used (Kennedy and Booth, 1951) displays patterns of plant preference consistent with published accounts of natural populations of A. fabae sensu stricto (Stroyan, 1987, Thieme, 1987, Blackman and Eastop, 1994). In preliminary experiments, individuals were reared in the laboratory on V. faba (see below) and tested on pre-flowering herbaceous summer host plants over 48 h in the ‘no choice’ situation (plants contained within a lamp glass with gauze lid). Winged
The initial plant recognition phase: host plants
Gynoparae on autumn-harvested spindle probed the plant tissue readily. Forty nine percent of the 63 untethered aphids that were placed on the plant penetrated before flight. This figure was comparable with that for the winged virginoparae on bean where 57% of 99 aphids probed (Fig. 1a). On all the other summer hosts plants of A. fabae, the winged virginoparae had a significantly lower incidence of tissue penetration (and a higher incidence of flight) relative to the gynoparae on
The central hypothesis: neural limitations
Decision-making on host plants does not seem to pose a problem for the generalist form of Aphis fabae analysed here. Few examples were found where the decision-making process of the generalist form is less efficient across host plants than the specialist on its host plant, E. europaeus, and decision making by the generalist is no less efficient than the specialist on the same host. In fact, in some cases, the generalist makes more efficient decisions on its host plant than the specialist on
Acknowledgements
This work was funded by the Biotechnology and Biological Sciences Research Council of the UK. Comments made by Prof. Sara Via during an informal discussion helped to improve the manuscript.
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