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Keywords:

  • interspecific hybrids;
  • oviposition;
  • insect-plant relations;
  • speciation;
  • diet breadth;
  • gustatory;
  • Yponomeutidae;
  • Lepidoptera;
  • Hopkins host selection principle

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Changes in host acceptance is an important factor in the host specialization of phytophagous insects, and knowledge of the genetic organization of this behaviour is necessary in order to understand how host shifts occur. Here we describe the inheritance of adult host acceptance (oviposition) in three closely related species of Yponomeuta Latreille (Lepidoptera: Yponomeutidae), and their interspecific hybrids. Yponomeuta cagnagellus (Hübner), a specialist on Euonymus europaeus L. (Celastraceae), Y. malinellus Zeller, a specialist on Malus spp. (Rosaceae), and Y. padellus (L.), oligophagous on a number of Rosaceae, were tested for their acceptance of parental hosts in choice tests. Acceptance of E. europaeus is semi-dominant in hybrids of Y. cagnagellus×Y. padellus, and in hybrids of Y. cagnagellus×Y. malinellus. The dominance of this acceptance was confirmed in oviposition tests with backcross hybrids: backcross hybrids F1 × Y. cagnagellus oviposited mainly on E. europaeus and F1 × Y. padellus still deposited more than half of their egg masses on E. europaeus. Reciprocal hybrids did not differ in their host acceptance, indicating that the trait is autosomal. We further studied the effect of larval food on adult host acceptance (‘Hopkins host selection principle’) in split full-sib F1 families. Larval diet influenced oviposition only in one of two hybrid crosses. The F1 hybrid of Y. padellus× Y. cagnagellus, reared on Prunus spinosa L., deposited a significantly lower percentage of egg masses on E. europaeus compared to their full-sib sisters fed with E. europaeus. We did not find this in the reciprocal cross. However, still more than half of the egg masses are deposited on E. europaeus by hybrids that have no experience on this host. We conclude that the semi-dominant character of acceptance of E. europaeus and a tendency of Rosaceae-feeding Yponomeuta to deposit egg masses on this host may have created the opportunity for the host shift of the predecessor of Y. cagnagellus from Rosaceae to the Celastraceae. This shift may have been further facilitated by a weak tendency of adults to oviposit on their larval food source.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

More than three-quarters of all described species are insects, the majority of which feed on plants. Many of these phytophagous insects are specialists, only feeding on one or a few related plant species (Schoonhoven et al., 1998). The colonization of, and subsequent specialization, on new – sometimes unrelated – host plants occurs frequently within insect species, and this is considered an important factor promoting insect speciation (Ehrlich & Raven, 1964; Mitter & Farrell, 1991; Dres & Mallet, 2002; Funk et al., 2002). There is growing support for the theory that host shifts, and subsequent speciation, can occur in sympatry in initially randomly mating populations (e.g., Bush, 1994; Coyne, 1994; Schluter, 2001; Via, 2001; Via & Hawthorne, 2002). The critical step in this process is the development of a linkage disequilibrium between several genes involved in adaptation to host plants, in spite of the homogenising effects of random mating and recombination. Empirical evidence indicates that ecology plays a key role in this process (Schluter & Nagel, 1995; Orr, 1998; Hatfield & Schluter, 1999; Groman & Pellmyr, 2000; de Mazancourt & Dieckmann, 2004). Mathematical modelling shows the likelihood of such ecological speciation, provided that some assortative mating takes place to counteract recombination between the adaptation genes (Felsenstein, 1981; Johnson et al., 1996; Kondrashov & Shpak, 1998; Dieckmann & Doebeli, 1999; Kondrashov & Kondrashov, 1999; Doebeli & Dieckmann, 2000; Via, 2001; Kirkpatrick & Ravigne, 2002). Although genes for host adaptation are important parameters in such models, detailed experimental data on the actual genetic basis of host adaptation is largely limited to some well-studied species such as those in the genus Drosophila (Jaenike, 1990; Coyne, 1992). Only recently, studies on other species including some Lepidoptera have appeared (Hawthorne & Via, 2001, and references therein). Clearly, we need information on the genetics of host adaptation from a broader set of insects to increase our understanding of the evolution of host associations in insect herbivores and of the effects host-plant shifts can have on speciation.

Host adaptation is a complex process, whose components most likely have separate genetic bases. A new host can be incorporated into an insect's diet if adults accept it for oviposition, larvae accept it for feeding, and the larvae are able to complete their life cycle on it. In this study, we use the term ‘host use’ to indicate the suite of adult and larval host acceptance and larval performance. To describe oviposition behaviour, we explicitly use the term ‘host acceptance’ in favour of the more common ‘host preference’ or ‘host choice’. The reason is that ‘acceptance’ simply denotes the observed behaviour, without making inferences about the hypothetical underlying mechanisms (Schoonhoven et al., 1998). Adult host acceptance is the basic constituent of host use in Lepidoptera, as first stadium larvae have little mobility and are generally unable to locate and migrate to a suitable food source if their mother chooses to oviposit on an unsuitable plant (Jermy, 1984; Miller & Strickler, 1984; Thompson & Pellmyr, 1991).

The main hurdle to studying the inheritance of host use is the general lack of suitable biological systems. A suitable system would be one that enables crosses between individuals specialized on different hosts, such as two populations of a species varying in host affiliations, or recently diverged species with differing host associations that have not yet evolved high levels of post-zygotic reproductive isolation (Coyne, 1992; Bush & Smith, 1998; K.H. Hora, F. Marec, P. Roessingh & S.B.J. Menken, unpubl.). Closely related species in the small ermine moth genus Yponomeuta Latreille (Yponomeutidae: Lepidoptera) provide such a system (Menken et al., 1992; Menken & Roessingh, 1998). In this model system we describe here the inheritance of adult host acceptance. We analyse the differences between three related Yponomeuta species feeding on Celastraceae and Rosaceae, which belong to different plant orders within the Eurosids I. Yponomeuta cagnagellus (Hübner) is specialised on Euonymus europaeus L. (Celastraceae), Y. malinellus Zeller is a specialist on Malus spp. (Rosaceae), and Y. padellus (L.) is oligophagous on several rosaceous plants, but is mainly found on Crataegus monogyna Jack. and Prunus spinosa L. (Menken et al., 1992). In the Netherlands, the three species do not hybridise in nature (Menken, 1980), but hybrids can be obtained in the laboratory. F1 hybrids develop well on both parental hosts, and do not show decreased fertility (K.H. Hora, F. Marec, P. Roessingh & S.B.J. Menken, unpubl.). Hybrids of these species can be viewed as artificial intermediate stages of host specialization on the two plant families enabling the study of inheritance of host use loci.

Adult host acceptance in Lepidoptera is controlled by the perception of leaf surface chemicals (Renwick & Chew, 1994). Lepidoptera will in general oviposit on artificial substrates if the appropriate leaf surface compounds are present. In Y. cagnagellus, it has been demonstrated that the surface extracts of host plants are sufficient to stimulate oviposition (Hora & Roessingh, 1999b), indicating that gustation is the principal mode of perception involved in adult host acceptance. In Y. padellus this is not yet known. A phytochemical basis of host acceptance behaviour provides an indication of the nature of the genes involved and suggests an evolutionary mechanism for host shifts through modifications in receptor proteins (Menken & Roessingh, 1998).

Besides being genetically determined, adult host acceptance behaviour could also be influenced by larval experience. A causal link between larval food experience and adult preference would facilitate host shifts (Hopkins, 1917). Such an epigenetic effect of larval food on adult oviposition has only been found in a few studies, given the number of attempts to find it (see Barron, 2001, for review) but it remains an interesting possibility in the context of the evolution of host acceptance.

Using interspecific hybrids, we address the following questions with regard to adult host acceptance:

  • 1
    Is adult host acceptance based on the perception of plant surface compounds?
  • 2
    How is adult host acceptance inherited?
  • 3
    Is there, in addition to genetic effects, also an induced epigenetic effect of larval diet on the adult host acceptance of F1 hybrids?

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Production of intraspecific controls, F1, and BC hybrid crosses

Insects for the production of interspecific hybrids and intraspecific crosses were collected in the field in the Netherlands as fifth instars on their host plants; Y. cagnagellus and Y. padellus in Wassenaar on E. europaeus and C. monogyna, respectively, and Y. malinellus in Amsterdam on M. domestica. Larvae were kept in glass jars (20 cm high, 11 cm diameter) or plastic cages (45 cm high, 20 cm diameter) at room temperature and under a natural light regime (June–July), and fed with fresh leaves of their hosts ad libitum until pupation. Pupae were put individually in glass vials (8 cm long and 2.1 cm in diameter), closed with cotton wool plugs, and stored at 18 °C (Y. padellus) or 24 °C (Y. cagnagellus and Y. malinellus) under a L16:D8 photoperiod. Yponomeuta cagnagellus and Y. malinellus reach sexual maturity about 2 weeks after eclosion, while Y. padellus takes about 1 week (Hendrikse, 1979). The higher storage temperature for Y. cagnagellus and Y. malinellus pupae thus synchronised their sexual development with that of Y. padellus.

Eclosed adults were sexed, and one male and one female were put in a vial for 1–2 weeks at 18 °C and under L16:D8. A solution of 1% vol/vol honey in water was provided in a 1% w/v agar medium. Males and females of the three species were combined to produce intraspecific crosses, reciprocal interspecific F1 hybrids, and backcross hybrids. Reciprocal backcross hybrids were made by crossing F1 (Y. padellus× Y. cagnagellus) (in all crosses the female parent is given first) with laboratory-reared Y. cagnagellus or Y. padellus. Gravid females of all cross types were individually allowed to oviposit in a no-choice situation on the twigs of potted plants in a greenhouse (20–25 °C, natural light regime of August–September), in Perspex cylinders (15 cm high and 4 cm in diameter, closed with cotton wool plugs at both ends), or in groups of five moths in cotton gauze sleeves (1 mm mesh size). Prunus spinosa was used for the oviposition of Y. padellus, as this is its preferred host (Gerrits-Heybroek et al., 1978; Kooi et al., 1991), Y. cagnagellus and F1 hybrid females were given E. europaeus, and Y. malinellus oviposited on M. domestica. Small ermine moths do not respond well to the manipulation of their univoltine life cycle. Therefore, the potted plants containing hibernacula of all cross types were stored in total darkness at 4 °C for a minimum of 4 months, creating an artificial winter diapause.

Rearing of intraspecific controls, F1, and BC hybrids

All laboratory-produced larvae were reared in plastic Petri dishes (2.5 cm high, 10 cm diameter) at 18 °C and under a L16:D8 photoperiod. Intraspecific crosses were given leaves of E. europaeus for Y. cagnagellus, P. spinosa for Y. padellus, and M. domestica for Y. malinellus. F1 hybrid larvae were provided with leaves of both parental hosts. Backcross hybrids were reared on the host of the backcross parent species. Sample sizes were kept at between 10 and 30 first stadium larvae per Petri dish. When larvae reached the L5 stage, the rearing groups were split into two if necessary, with a maximum of 15 L5 per Petri dish. This procedure ensured that larvae could feed ad libitum at all times, and that L5 larvae of all species had similar group sizes (between 10 and 15).

After pupation, cocoons were put individually into clean glass vials. Eclosed adults were treated in the same manner as their parents prior to the oviposition experiments. Each female was mated to a brother or – sporadically – to a male of another family, but of the same cross type and larval diet.

Inheritance of adult host acceptance

Host acceptance of F1 and backcross hybrids was compared under dual choice conditions on the two parental (F1) or grandparental (BC) host plants, i.e., E. europaeus and P. spinosa for hybrids between Y. cagnagellus and Y. padellus, and E. europaeus and M. domestica for hybrids between Y. cagnagellus and Y. malinellus. Mated females were placed in Perspex cylinders (15 cm high, 4 cm diameter) and offered either twigs of potted plants in the greenhouse at L16:D8 (Hora & Roessingh, 1999b) or cut-off twigs of both hosts, kept fresh in separate vials containing a 1% w/v agar solution in a growth chamber at 24 °C and L16:D8 (Hora & Roessingh, 1999b).

Usually, females were allowed to oviposit individually. In some instances we chose to use two females per cage due to a shortage of plants or cages (see Tables 1–4 for details on the number of insects). Twigs of potted plants were passed through the Perspex cylinders, and both ends of the cylinder were closed with cotton wool plugs, which also served to keep the two twigs approximately 3 cm apart. In order to avoid a high humidity in the cage, and to enable the counting of egg masses during the experiment, leaves were removed from the twigs at least 24 h before the introduction of the moths.

Table 1.  Percentage of total egg masses (mean and 95% confidence limits) deposited on E. europaeus by Yponomeuta cagnagellus (cag), Yponomeuta padellus (pad), and their reciprocal F1 hybrids in choice situations between E. europaeus and Prunus spinosa. (A) Twigs of potted plants, (B) Cut twigs, and (C) Artificial twigs with host extract. Different letters indicate significant differences between maximally non-significant sets determined by G-tests with the simultaneous test procedure
CrossNumber ofNumber of egg masses on% of egg masses on E. europaeus95% confidence limits
cagesfemalesE. europaeusP. spinosa
  • a

    G-tests: G = 23.77, d.f. = 3, P<0.001; G = 0.656, d.f. = 3, ns for the crosses indicated with b.

  • b

    G-tests: G = 140.2, d.f. = 3, P<0.001; G = 30.84, d.f. = 3, P<0.001 for the crosses indicated with b and c and G = 2.05, d.f. = 3, ns, for the crosses indicated with b.

  • c

    G-tests: G = 40.45, d.f. = 3, P<0.001; G = 4.39, d.f. = 3, ns for the crosses indicated with a.

(A) Potted plantsa
 cag × cag1919 68 0100 a94–100
 F1 pad × cag375212324 84 b77–89
 F1 cag × pad1720 38 8 83 b72–93
 pad × pad4447 7820 80 b71–87
(B) Cut twigsb
 cag × cag3333 62 1 98 a91–100
 F1 pad × cag6969 8541 67 b58–75
 F1 cag × pad3939 9631 76 b68–83
 pad × pad4545 1677 17 c10–26
(C) Artificial twigs with host extractc
 cag × cag 524 13 0100 a78–100
 F1 pad × cag1152 36 8 82 a68–91
 F1 cag × pad38 8 44 8 85 a73–93
 pad × pad 737 1327 33 b20–49
Table 2.  Percentage of total egg masses (mean and 95% confidence limits) deposited on cut twigs of E. europaeus by Yponomeuta cagnagellus (cag), Yponomeuta malinellus (mal), and their reciprocal F1 hybrids in choice situations between E. europaeus and Malus domestica. Different letters indicate significant differences between maximally non-significant sets determined by G-tests with the simultaneous test procedure
CrossNumber ofNumber of egg masses on% of egg masses on E. europaeus95% confidence limits
cagesfemalesE. europaeusM. domestica
  1. G-tests: G = 33.84, d.f. = 3, P<0.001; G = 14.08, d.f. = 3, P<0.005 for the crosses indicated with a and b and G = 1.039, d.f. = 3, ns, for the crosses indicated with b.

cag × cag333361 198 a91–100
F1 mal × cag1919331077 b62–88
F1 cag × mal263950 985 b74–92
mal × mal 613 2 820 c 2–55
Table 3.  Percentage of total egg masses (mean and 95% confidence limits) deposited on E. europaeus by Yponomeuta cagnagellus (cag), Y. padellus (pad), and their backcross hybrids with F1 in choice situations between E. europaeus and Prunus spinosa. The ×× sign indicates that the reciprocal F1 crosses were combined. Different letters indicate significant differences between maximally non-significant sets determined by G-tests with the simultaneous test procedure
CrossNumber ofEgg masses on% of egg masses on E. europaeus95% confidence limits
cagesfemalesE. europaeusP. spinosa
  1. G-tests: G = 147.4, d.f. = 3, P<0.001; G = 57.22, d.f. = 3, P<0.001 for the crosses indicated with a, b, and c; G = 85.59, d.f. = 3, P<0.001 for the crosses indicated with a, b, and d; G = 17.01, d.f. = 3, P<0.05 for the crosses indicated with b and c.

cag × cag3030120 0100 a97–100
BC cag ×× F1525216727 86 b80–90
BC pad ×× F12020 2720 57 c40–67
pad × pad2020  331  9 d 3–21
Table 4.  Percentage of total egg masses (mean and 95% confidence limits) deposited on E. europaeus by F1 hybrids of Yponomeuta cagnagellus (cag) and Y. padellus (pad) reared on either E. europaeus or Prunus spinosa in choice situations between E. europaeus and Prunus spinosa. (A) F1 cag × pad and (B) F1 pad × cag. Different letters indicate significant differences between maximally non-significant sets determined by G-tests with the simultaneous test procedure
CrossReared onNumber ofEgg masses on% of egg masses on E. europaeus95% confidence limits
cagesfemalesE. europaeusP. spinosa
  • a

    G-test: G = 0.546, d.f. = 1, ns.

  • b

    G-test: G = 12.44, d.f. = 1, P<0.01.

(A)a
F1 cag × padE. europaeus63731791791 a86–94
P. spinosa51661111489 a79–91
(B)b
F1 pad × cagE. europaeus66851865178 a72–83
P. spinosa3951 604159 b49–69

To determine if host acceptance of the hybrids was mediated by plant surface compounds, which are known to affect oviposition in Y. cagnagellus (Hora & Roessingh, 1999b), hybrids and parental species were also tested on artificial twigs treated with surface compounds, extracted in methanol from E. europaeus and P. spinosa twigs. The artificial twigs were constructed from glass Pasteur capillary pipets (150 mm long × 7 mm outer diameter), covered with paper tape, and placed per pair (one for each extract) in a Perspex cylinder (15 cm high, 4 cm diameter). Extracts were applied on the artificial twigs in concentrations comparable to those extracted from a similar surface of twigs, i.e., one Twig Surface Equivalent (Hora & Roessingh, 1999b). We combined 4–6 females per cage (Table 1).

Because F1 hybrids between Y. malinellus and Y. cagnagellus, and intraspecific crosses of Y. malinellus are not easily obtained in large numbers, the oviposition of F1 hybrids with Y. malinellus was only tested on cut-off twigs of E. europaeus and M. domestica.

Influence of larval diet on adult host acceptance

Pupae were taken out of their cocoons within 5 days of pupation, and placed in clean glass vials, to exclude ‘early adult experience’ (Corbet, 1985) via contamination of the pupal surface and the glass vials with plant compounds or frass. For the oviposition experiment, full-sib females of reciprocal hybrid crosses between Y. cagnagellus and Y. padellus, reared on either of the two parental hosts, were offered a choice between E. europaeus and P. spinosa twigs of potted plants, as described for the previous experiment. This experiment was done in three replicates in three consecutive years.

To avoid an effect on adult host acceptance caused by genetic variability among groups of moths reared on either diet, we used a split family design by dividing first instars from one egg mass (full-sib family) in two samples of equal size, and reared each sample on either E. europaeus or P. spinosa in the same manner as described above under ‘Rearing of intraspecific controls, F1, and BC hybrids’. Mortality on both host plants was similar to that of the parental species (K.H. Hora, P. Roessingh & S.B.J. Menken, unpubl.) indicating that the effects of the diet on oviposition are not likely to be a result of selection in the larval stage.

Analysis

Host acceptance was quantified by counting the number of egg masses deposited on the different oviposition substrates during the full female life span. Egg mass counts were pooled over cages and cross types and a single proportion of egg masses on E. europaeus was calculated. Significant differences in preference between cross types were determined using the G-test with William's adjustment for low cell numbers. If significant differences were found, the simultaneous test procedure (Sokal & Rohlf, 1995) was applied to determine maximally non-significant sets (indicated with letters behind the proportions in the tables). Different letters indicate significant differences. In addition, the shortest unbiased 95% confidence limits for each proportion were calculated (Rohlf & Sokal, 1995).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Effects of oviposition substrate on egg mass size

To control for the effect of the oviposition substrate on the size of the egg masses, the number of eggs per egg mass was counted in one of the three replicates of the experiment. Oviposition substrate did not influence the size of an egg mass: the number of eggs per egg mass was not significantly different for masses on E. europaeus (mean ± SE = 51.4 ± 1.9; n = 258) or P. spinosa (mean ± SE = 48.4 ± 3.2; n = 71) (Mann–Whitney, P>0.05). Therefore, we used egg mass count rather than egg count as the dependent variable in all analyses.

Inheritance of adult host acceptance

Oviposition of F1 hybrids on twigs of potted plants, cut twigs, and artificial twigs with host extracts, followed the same pattern (Table 1). Reciprocal crosses between Y. padellus and Y. cagnagellus did not show significant differences in their acceptance of E. europaeus (G-test: d.f. = 3, G = 0.656, 2.05, and 0.132 for the three treatments respectively, all non-significant). Over all experiments between 67% and 85% of the egg masses was deposited on that host, and thus 33–15% on P. spinosa (Table 1). Both reciprocal hybrids of Y. cagnagellus and Y. malinellus showed a similar (77–85%, Table 2) and not significantly different acceptance of cut twigs of E. europaeus (G-test: G = 1.025, d.f. = 3, ns). Host acceptance of intraspecific Y. cagnagellus, Y. padellus, and Y. malinellus was generally significantly different from that of the hybrids (Tables 1 and 2; see all Tables for the values of the test statistics). Yponomeuta cagnagellus oviposited almost exclusively on its own host E. europaeus. Over all experiments, only two egg masses were laid on a non-host. As expected, Y. padellus mainly accepted its host P. spinosa, but in contrast to Y. cagnagellus, egg masses were also deposited on the non-host E. europaeus. The percentage of mislaid egg masses was less on cut than on artificial twigs (17% and 33%, respectively; Table 1B, C). It was very high on twigs of potted plants (80%: Table 1A). As a consequence, and in contrast to all other experiments, host acceptance of the F1 hybrids of twigs of potted E. europaeus (Table 1A) was not significantly different from that of ‘pure’Y. padellus (G-test: G = 0.656, d.f. = 3, ns). Similar to Y. padellus, Y. malinellus deposited 20% of the egg masses on the non-host E. europaeus (Table 2).

As there was no significant difference in host acceptance between the reciprocal backcross hybrids for Y. cagnagellus and Y. padellus (data not shown), the reciprocals were pooled. Reciprocal backcross hybrids with Y. cagnagellus (BC cag xx F1) preferred E. europaeus (see Table 3 for values of test statistics) but still oviposited 14% (Table 3) of their egg masses on P. spinosa. Both backcross hybrids with Y. padellus as either male or female (BC pad xx F1) deposited egg masses equally on both E. europaeus (57%) and P. spinosa (42%) (Table 3).

Influence of larval diet on adult host acceptance

In the experiment that evaluated the influence of larval diet on adult host acceptance (Hopkins host selection principle), the F1 cag × pad hybrids, reared on P. spinosa, did not significantly differ from their full-sib sisters reared on E. europaeus (89% vs. 91% oviposition on E. europaeus; Table 4A; G-test: G = 0.546, d.f. = 3, ns). In contrast, the reciprocal F1 pad × cag hybrids, reared on P. spinosa, deposited a significantly lower percentage of egg masses on E. europaeus compared to their full-sib sisters fed with E. europaeus (59% vs. 78%; Table 4B, G-test: G = 12.44, d.f. = 3, P<0.01). This result suggests an effect of the larval diet of P. spinosa on later oviposition.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Inheritance of adult host acceptance

In this study we showed that interspecific hybrids of Y. cagnagellus×Y. padellus and Y. cagnagellus×Y. malinellus preferred E. europaeus (the host of Y. cagnagellus) for oviposition, but each cross also accepted the host of the other parent (i.e., P. spinosa for Y. padellus and M. domestica for Y. malinellus). Backcross hybrids with Y. padellus as parent still readily accepted E. europaeus. It can therefore be concluded that acceptance of E. europaeus is semi-dominant. F1 hybrids produced from reciprocal interspecific crosses did not show a difference in host acceptance (Tables 1 and 2), indicating that in Yponomeuta the genes controlling host acceptance are not sex-linked.

In Lepidoptera, studies into the genetics of host acceptance behaviour are scarce, as it is often not feasible to obtain the large sample sizes or balanced experimental designs needed for a detailed analysis. However, it appears that variation in adult host acceptance in general is heritable and responsive to selection (Tabashnik et al., 1981; Singer et al., 1988; Thompson et al., 1990; Waldvogel & Gould, 1990; Thompson & Pellmyr, 1991; Bossart & Scriber, 1995; Janz, 1998). Most of the studies considered the inheritance of variation in the ranking of hosts within a species. Interspecific hybrids have been used to study host ranking between Papillio species, where the trait was found to be sex-linked (Thompson et al., 1990). In Heliothis species, however, host acceptance appears to be autosomal (Schneider & Roush, 1986; Sheck & Gould, 1995) In Yponomeuta, crosses between Y. malinellus and Y. cagnagellus also showed autosomal and dominant inheritance of sensitivity to the sugar alcohols ducitol and sorbitol, which are major feeding stimulants for these species (van Drongelen & van Loon, 1980).

Female Yponomeuta F1 hybrids are expected to possess autosomal alleles for the acceptance of both parental hosts and, in the case of sex-linkage, Z-linked alleles for acceptance of their father's host (females are the heterogametic sex in Lepidoptera, and X and Y are named Z and W, respectively). Our finding that host acceptance in Yponomeuta is apparently autosomal contrasts with the strong bias toward sex linkage of genes that code for species differences in Lepidoptera (Sperling et al., 1995; Pashley-Prowell, 1998). In the 11 best-studied lepidopteran species complexes, more than half of all ecological, behavioural, or physiological differences among species are controlled by genes located on the Z chromosome. The common explanation for this preponderance of sex linkage is based on the lack of recombination in the heterogametic sex. The accumulation of gene complexes on the Z chromosome could facilitate host shifts, because in the heterogametic sex co-adaption of multiple host use, loci would not be disrupted by recombination (Hagen & Scriber, 1995). However, it is unclear why this phenomenon should be especially pronounced in Lepidoptera (Pashley-Prowell, 1998), since in this insect order female autosomes do not undergo recombination either (Traut & Marec, 1996; Raijmann et al., 1997), and linkage groups will therefore be favoured equally on autosomes and sex chromosomes.

Charlesworth et al. (1987) showed that the rate of evolution of favourable autosomal mutations exceeds that of X-linked loci if they are semi-dominant or dominant, especially if selection acts on the heterogametic sex. If traits on the X-chromosome lack dosage compensation, the rate of evolution for autosomal genes will even exceed that for X-linked genes when the degree of dominance is higher than 0.25. Obviously, oviposition is a trait expressed – and thus selected for – only in the heterogametic female moths, and Lepidoptera are known to lack dosage compensation (Traut & Marec, 1996). From this perspective, our finding that host acceptance in Yponomeuta is an autosomal trait is not unexpected. The importance of the Z chromosome for speciation in Lepidoptera is possibly biased by the scant reports on the genetics of species differences with examples from a limited number of families (Sperling et al., 1995; Pashley-Prowell, 1998).

Oviposition in Lepidoptera is largely mediated by specific non-volatile host compounds perceived by gustatory sensilla (Renwick & Chew, 1994; Schoonhoven et al., 1998). In Y. cagnagellus, for instance, adult host acceptance is based on non-volatile plant-surface chemicals (Hora & Roessingh, 1999a,b). In the present paper, we show that this is also the case for the closely related Y. padellus. This species preferred to lay its egg masses on artificial twigs treated with host extract compared to twigs treated with an extract of the non-host E. europaeus. Interspecific hybrids also accepted artificial substrates treated with E. europaeus twig-surface extracts more often than a P. spinosa twig-surface extract. This shows that host acceptance in Y. padellus is based on non-volatile plant-specific surface compounds, and that it has a genetic basis. The genes involved in this trait might code for receptor proteins (or proteins in the associated signalling cascade) used for perception of these compounds. Alternatively, the trait might be controlled by unknown factors affecting the processing of peripheral information in the central nervous system (Menken & Roessingh, 1998).

An alternative explanation for the results presented here could be that part of the egg masses deposited by the hybrids were not due to acceptance behaviour inherited from Y. cagnagellus, but were instead due to a lower host fidelity inherited from Y. padellus (Table 1B). However, from the combined results of this study it is clear that the acceptance of E. europaeus can be easily crossed into an Y. padellus population, whereas the introduction of acceptance of P. spinosa into an Y. cagnagellus population is more difficult. This result might reflect the ancestral relation with Celastraceae (see below).

Influence of larval diet on adult host acceptance

In addition to genetic effects, host acceptance of the hybrid female Yponomeuta appears to be influenced by larval diet. Host acceptance of F1 hybrids with Y. padellus as mother was altered when fed with P. spinosa: females deposited significantly more egg masses on P. spinosa than their sisters which had been reared on E. europaeus (Table 4B). However, larval experience did not induce a radical change in host acceptance. F1 pad × cag hybrids – without experience with E. europaeus– still deposited more than half of their egg masses on this host (Table 4). This confirms that, although the trait shows some plasticity, it does have a considerable heritable component. Studies into the effect of larval diet on oviposition in moths are rare, and the outcomes contradictory (cf. Barron, 2001). In Spodoptera littoralis, females ensuing from a potato-based diet were more inclined to accept this diet than females which had not been raised on that diet (Anderson et al., 1995). Furthermore, Manduca sexta reared on jimson-weed or tobacco preferably accepted the plants on which they were reared (Yamamoto et al., 1969). Finally, oviposition of host races of the codling moth, Laspeyresia pomonella, was affected by larval diet (Phillips & Barnes, 1975). However, the cabbage moth, Mamestra brassicae, did not change its adult host acceptance in response to larval diet (Rojas & Wyatt, 1999), and neither did Ostrinia nubilalis, Papilio machaon, or Helicoverpa zea (Thompson & Parker, 1928; Palmiter, 1966; Wiklund, 1974).

We have found a difference in the effects of larval diet on adult host acceptance in reciprocal Yponomeuta F1 interspecific hybrids; a P. spinosa diet only affected host acceptance when Y. padellus was the maternal parent (F1 pad × cag; Table 4B). Since the eggs for the crosses were laid on the host of the mother, F1 pad × cag hybrids all experienced P. spinosa at the very beginning of their first larval stage (Yponomeuta larvae hatch under a hibernaculum in the summer, and may eat small amounts of bark before they emerge from under this protective shield in the spring). On the other hand, we cannot exclude the possibility that the effect of the larval diet is located on the W-chromosome of Y. padellus. This chromosome is inherited from the mother, and would be exclusively present in F1 pad × cag hybrids. There is little evidence that heterochromatinous lepidopteran W-chromosomes carry genetic information (Goldsmith & Wilkins, 1995; Traut & Marec, 1996), however, W-linked genes can not be fully excluded (e.g., Guelin, 1994).

Implications for the evolution of Yponomeuta host affiliations

Host shifts are viewed as an important step in sympatric speciation. Disruptive selection acting on resource use in populations of oligophages is expected to be one of the prime factors driving host shifts and specialisation. The process may involve genetic, physiological, or ecological trade-offs which will eventually direct selection for assortative mating within host races (Jaenike, 1990; Futuyma, 1991; Jermy, 1993; Denno et al., 1995; Joshi & Thompson, 1995; Feder, 1998; Dieckmann & Doebeli, 1999). However, disruptive selection can only take place after the new host has been incorporated into the insect's diet. In this discussion we focus on the first step in host shifts: acquisition of the host use traits enabling colonisation of the new host.

The great majority of Yponomeuta species feed on Celastraceae, reflecting a primary association with this plant family (Menken, 1996; S.A. Ulenberg, unpubl.). Molecular phylogenetic analyses indicate that in Europe a unique shift has taken place from Celastraceae to Rosaceae and further on to Salicaceae (H. Turner, N. Lieshout, W. van Ginkel & S.B.J. Menken, unpubl.). Although Y. cagnagellus falls within this European clade, it feeds on E. europaeus, and thus this species actually represents a backshift from Rosaceae, and its association with Celastraceae is therefore secondary.

Oviposition on a celastraceous host by a Rosaceae-specialist is a prerequisite for a host shift from Rosaceae to Celastraceae. We have found that Y. padellus, and to a lesser extent Y. malinellus, will accept E. europaeus for oviposition (Tables 1 and 2, and Geerts et al., 2000). A Rosaceae-feeding ancestor of Y. cagnagellus carrying the gene(s) for this trait would be pre-adapted to a backshift to Celastraceae. Furthermore, if E. europaeus occurred in sympatry with rosaceous hostplants, as it does today, there would also have been the ecological opportunity for a backshift.

The ambiguous oviposition behaviour (cf. Larsson & Ekbom, 1995) of Y. padellus seems to be non-adaptive, since its larvae cannot complete their life cycle on E. europaeus (Kooi et al., 1991; K.H. Hora, P. Roessingh & S.B.J. Menken, unpubl.). It is possibly a side-effect of the oligophagous feeding of Y. padellus and the high variation of suitability of its hosts (Fung, 1989). With the ability to recognise a wider range of hosts, with variable suitability, a certain imperfection in host discrimination might be unavoidable (Kooi et al., 1991; Fox & Lalonde, 1993; Larsson & Ekbom, 1995). In addition, E. europaeus is the only representative of the Celastraceae in Europe, and far less abundant than the rosacaeous Yponomeuta hosts. This ecological factor may impede the evolution of the perfect host discrimination of Rosaceae feeders, and avoidance behaviour will not easily evolve (Rausher, 1985).

The frequent host shifts associated with speciation in Yponomeuta species (S.A. Ulenberg, unpubl.) imply that specialisation is not an evolutionary dead-end (see Janz et al., 2001, for a discussion of this idea). Even highly specialized species seem to contain sufficient genetic variation to allow selection for host shifts (Futuyma et al., 1993). Moreover, a reversion to E. europaeus, similar to the ancestral host, may occur more readily than the adoption of an entirely new host. The genes that governed the use of celastraceous hosts may not have been completely lost in the Rosaceae feeders (Mitter & Farrell, 1991; Janz et al., 2001) and possibly facilitated the evolution of a larval ability to thrive on Euonymus following frequent oviposition ‘mistakes’ on Euonymus.

As suggested before, genes for the acceptance of E. europaeus can easily be introduced into a population of Rosaceae-feeding moths. This means that once the offspring of females with a genetic predisposition to accept E. europaeus for oviposition are able to survive on that host, adult host acceptance for E. europaeus may rapidly spread in the population. Next, genes for adult host acceptance and those for larval performance have to become correlated in one way or another in order for the host race to become evolutionarily successful. It seems unlikely that adult host acceptance is already genetically linked with larval performance: backcross hybrids with Y. padellus as the backcross parent frequently oviposit on E. europaeus, but only 7% survive on this host (K.H. Hora, P. Roessingh & S.B.J. Menken, unpubl.). An influence of larval food might further facilitate the building of an association between larval and adult acceptance traits. In addition, this association may be facilitated by the fact that E. europaeus has higher nitrogen and water contents than P. spinosa (Fung, 1989), and probably therefore a higher nutritional value. F1 hybrids reared on E. europaeus have a lower mortality and reach higher pupal weights than on P. spinosa (K.H. Hora, P. Roessingh & S.B.J. Menken, unpubl.). The colonization of E. europaeus could therefore be beneficial to the individual by directly increasing its fitness. This provides a selective advantage, possibly resulting in linkage disequilibrium between preference and performance genes. Disruptive selection favouring specialists on the new host could then act on individuals able to choose the new host, and complete their life cycle on it.

We conclude that the semi-dominant nature of acceptance of E. europaeus and a tendency of Rosaceae-feeding Yponomeuta to deposit egg masses on this host could have facilitated the return to a celastraceous host of Y. cagnagellus in Europe. This backshift may have been further facilitated by a weak tendency of adults to oviposit on their larval food source, as is demonstrated by the present-day Y. padellus.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We thank Hans Breeuwer for his useful comments on this manuscript in its early stages, and Wil van Ginkel for help with the cultures. The investigations were supported by the Life Sciences Foundation (S.L.W.), which is subsidised by The Netherlands Organisation for Scientific Research (NWO).

References

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  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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