Evolution of host range and life history
The majority of Orobanche and Phelipanche species have a narrow host range and grow on perennial hosts (Beck-Mannagetta, 1930; Uhlich et al., 1995; Teryokhin, 1997). An association between parasite specialization and resource predictability (host longevity) is expected (Ward, 1992). This has been repeatedly shown for animal parasites, e.g. fleas or monogenean flatworms (Krasnov et al., 2006; Šimkováet al., 2006), and is suggested here for parasitic plants. It is likely that host recognition, being the first phase of host–parasite interaction, is important for this distribution of life traits. Host recognition comprises several steps, which are all equally important for the successful establishment of a connection to the host, such as germination and haustorium formation (Bouwmeester et al., 2003). Each step invokes chemical signalling between the host and the parasite. For example, seed germination and haustorium development occur only after stimulation by chemical signals released by the host (xenognosins; Atsatt et al., 1978; Keyes et al., 2001; Yoder, 2001; Bouwmeester et al., 2003). Each step can determine host specificity and thus host range, e.g. a plant might produce germination stimulants and hence induce germination of the parasite, but may be resistant in later stages of the parasite's lifecycle (e.g. Chittapur et al., 2001). For obligate parasites, which entirely depend on their hosts, it is crucial to specifically respond to signals from the correct hosts to maximize the chances of a successful establishment of a connection. One would therefore expect most Orobanche and Phelipanche species to be very specific and grow only on a few host species to which they are well adapted, and thus to have narrow host ranges. Although annual plants are suitable hosts due, for example, to weaker lignification of host tissue allowing easier penetration, or to decreased defence mechanisms compared with perennials (Feeney, 1976; Coley et al., 1985), they impose severe time constraints on the parasite's development. These time constraints might explain the prevalence of perennial hosts.
From the available data it is not possible to infer the temporal sequence of character state transitions. Using a parsimony based method of character state reconstruction, it has been suggested that the ancestral character states are narrow host range and perennial life history (Manen et al., 2004; G. M. Schneeweiss, unpublished). This fits the scenario outlined above, which suggests that holoparasitic plants are expected to be well adapted to a few host species only. However, the maximum-likelihood method employed here reveals that the ancestral character states are totally ambiguous, that is, each of the four trait combinations in the model of correlated evolution has a probability of 0.25 (data not shown).
A possible mechanism involved in changes of host ranges is a heritable polymorphism in response to xenognosins, as is known for the hemiparasitic Orobanchaceae Triphysaria pusilla (Jamison & Yoder, 2001). This can result in the formation of intraspecific host races, as is suggested from glasshouse experiments for Orobanche and Phelipanche (Musselman et al., 1981; Boulet et al., 2001). These studies do not directly focus on this question, however, and further experiments incorporating more Orobanche strains are required. Other scenarios, such as changes in the xenognosin receptor(s) or changes in the required threshold of xenognosins, concerning both duration of exposure (Chang & Lynn, 1986; Smith et al., 1990) and quantity of exudates, are currently not testable because of insufficient data.
The reasons for the association between wide host range and annual life history are elusive. One hypothesis is that with an increasing number of potential host species the probability of attacking annual hosts simply increases as well. If correct, a positive correlation between number of attacked host species and number of annual host species is expected, which could be tested if sufficiently detailed and correct data were available. A second hypothesis is based on the proposal that species with a wide host range have a higher chance of finding a suitable host than species with a narrow host range, and will therefore generally have larger populations. It may be that in the transitional phase from perennial to annual hosts a considerable number of parasites, being not yet perfectly adapted, are not able to finish their life cycle on annual hosts. This loss of offspring is expected to be less critical in larger populations. Although demographic data of species with contrasting trait combinations would allow us to test this hypothesis, such data, at least for natural habitats, are lacking. In man-made or anthropogenically disturbed habitats, species with wide host range and annual life history often occur in large numbers, but it is unclear if this is because of the life traits or because of specific conditions of the habitats. Host unpredictability because of low host abundance has been suggested to favour parasite generalists (Norton & Carpenter, 1998; Tripet et al., 2002), and host longevity (annual life history) may play a similar role (Šimkováet al., 2006). Facultative autogamy is known for several weedy Orobanche and Phelipanche species (Musselman et al., 1981), and this pollination mode may play an important role in the fixation of mutations advantageous for growing on annual hosts. Comparative studies using closely related species with contrasting life traits, such as those in the clade comprising O. minor and its relatives (Fig. 1b), would clearly help to address such questions.
Evolution of weediness
Of the approximately 170 species of the genera Orobanche and Phelipanche, few are weedy species (e.g. Orobanche picridis, Phelipanche mutelii, P. nana) and only five have become major pests (Orobanche crenata, O. cumana, O. minor, Phelipanche aegyptiaca, P. ramosa; Parker & Riches, 1993; Riches & Parker, 1995; Teryokhin, 1997). These taxa share wide host ranges and annual life histories, whereas the majority of Orobanche and Phelipanche species have narrow host ranges and perennial life histories (Table S1). This suggests that these traits play an important role in the evolution of weediness in Orobanche and Phelipanche. It is obvious that annual life history is an obligate prerequisite for a parasite growing on annual host plants, which usually dominate in anthropogenically disturbed habitats such as agricultural fields. The role of wide host range in virulent Orobanche races is less clear, although it might indirectly facilitate the evolution of annual life history.
Several factors warrant caution in the interpretation of the above results. These include the incompleteness of sampling, which can affect the distribution of character states along the phylogeny and thus bias the estimation of rate parameters. For example, unsampled species might have trait combinations not encountered in the current data set, or species belonging to well-defined clades within their respective genera might show trait combinations differing from their close relatives. This situation is complicated by the taxonomic uncertainty of the species, especially in less explored regions such as Near and Central Asia, where major components of the species diversity of both Orobanche and Phelipanche reside (Beck-Mannagetta, 1890, 1930; Teryokhin et al., 1993; Uhlich et al., 1995).
Several potential biases stemming from the method used have been recently addressed in the context of ecological specialization of insects (Nosil & Mooers, 2005; Stireman, 2005). These include, for example, higher transition rates to the more common state. Currently implemented methods of character state reconstruction assume that the rate of character change is the same in each group over the whole phylogeny. The actual distribution of character states in both Orobanche and Phelipanche would, however, suggest the presence of rate heterogeneity. For instance, in Orobanche, species with annual life history are confined to two clades (O. cernua s.l., O. minor and related species), which significantly also include very closely related taxa with perennial life history. The situation is similar to that of a molecular clock in models of sequence evolution, which has been found to be violated in most of the real data sets (Bromham & Penny, 2003; Renner, 2005). It is expected that in analogy to local molecular clock or relaxed molecular clock approaches (reviewed in Renner, 2005; Welch & Bromham, 2005), future models of character evolution will allow variation in the rate of character change.