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Keywords:

  • ecological specialization;
  • host shift;
  • parasites;
  • relaxed selection;
  • trade-off

Abstract

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

Using experimentally induced disruptive selection, we tested two hypotheses regarding the evolution of specialization in parasites. The ‘trade-off’ hypothesis suggests that adaptation to a specific host may come at the expense of a reduced performance when exploiting another host. The alternative ‘relaxed selection’ hypothesis suggests that the ability to exploit a given host would deteriorate when becoming obsolete. Three replicate populations of a flea Xenopsylla ramesis were maintained on each of two rodent hosts, Meriones crassus and Dipodillus dasyurus, for nine generations. Fleas maintained on a specific host species for a few generations substantially decreased their reproductive performance when transferred to an alternative host species, whereas they generally did not increase their performance on their maintenance host. The results support the ‘relaxed selection’ hypothesis of the evolution of ecological specialization in haematophagous ectoparasites, while suggesting that trade-offs are unlikely drivers of specialization. Further work is needed to study the extent by which the observed specializations are based on epigenetic or genetic modifications.


Introduction

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

Studying the evolution of ecological specialization is pivotal for our understanding of adaptive radiations and biological diversity (e.g. Futuyma & Moreno, 1988; Thompson, 1994; Fry, 1996; Desdevises et al., 2002; Devictor et al., 2010; Poisot et al., 2011). However, in spite of numerous studies (Bradshaw, 1965; Levins, 1968; Futuyma & Moreno, 1988; Thompson, 1994; Bolnick et al., 2003; Ravignéet al., 2009; Poisot et al., 2011), important aspects of the evolution of ecological specialization and its functional alternatives are yet to be experimentally explored. Specifically, it is usually not clear what dictates the interplay and trade-offs between the abilities of an organism to exploit different resources or the frequently observed negative correlations between the organism’s ability to exploit a wide range of resources and its performance when exploiting each one of them individually (e.g. MacArthur, 1972; Futuyma & Moreno, 1988; Pianka, 2000; Vanhooydonck et al., 2001; Kassen, 2002; Roff & Fairbairn, 2007; Dennis et al., 2011).

Parasites represent a convenient model system for studying the evolutionary ecology of specialization due to the discreteness and clarity with which they express host preference and specificity (e.g. Poulin et al., 2011). Moreover, understanding the evolution of parasite specialization is particularly important for understanding the distribution and spread of zoonotic diseases and the development of theoretical frameworks and applied protocols for their prevention and eradication (e.g. Krasnov et al., 2006; Agosta et al., 2010).

Parasite host specificity is greatly variable (Marshall, 1981; Poulin, 2007) although highly conservative both ecologically and evolutionary (Brooks & McLennan, 1991; Thompson, 1994, 2005). Interestingly, the great majority of parasites are host-specific and true generalists are relatively rare (Lajeunesse & Forbes, 2002; Poulin et al., 2006a). The reasons for the scarceness of host opportunists could be the costs incurred by the ability to exploit multiple hosts (Wilson & Yoshimura, 1994). Namely, adaptations to a specific host may come at the expense of reduced performance on another host, as suggested by both theoretical models (e.g. Regoes et al., 2000; Gandon, 2004) and empirical studies (Zovi et al., 2008; but see Jaenike & Dombeck, 1998). In addition, host specialization can also result in decreased abilities to exploit multiple hosts, that is, due to a specialization–generalism trade-off (Fry, 1990a,b; Ward, 1992; Poulin, 1998; Woolhouse et al., 2001; but see Barger & Esch, 2002; Krasnov et al., 2004a). However, it has been suggested that these trade-offs are mainly important in sequential hosts of parasites with complex life cycles, where a parasite specializes on two or more hosts and partitions this specialization to different stages of its life cycle (Davies et al., 2001; Gower & Webster, 2004; Poulin, 2007; Rigaud et al., 2010). It remains unclear whether such trade-offs occur when multiple hosts are exploited by parasites synchronously rather than sequentially(that is, parasites with direct life cycle or at the same developmental stage) (Combes, 2001; Gandon, 2004; Rigaud et al., 2010). Moreover, it was suggested that owing to trade-offs between the performances in different hosts, specialization might turn into a ‘one-way ticket’ to further specialization and limited diversification (Mayr, 1963; Jaenike, 1990). However, later studies demonstrated that generalist parasites often have specialized ancestors (Radtke et al., 2002; Poulin et al., 2006a,b) and that the evolution of ecological specialization has no intrinsic direction (Thompson, 1994). Another scenario for evolutionary increase in host specificity may be the existence of constant directional selection on specific traits. However, when encounter rates with a specific host are low, due to decreasing abundances or complete extinctions, a parasite may lose its specific adaptations to a host due to relaxed selection, that is, when these adaptations becomes obsolete either locally or globally. Although the two scenarios (specialization trade-offs and relaxation of selection) may promote both adaptive specialization and genetic diversity, their underlying evolutionary mechanisms are contrasting.

To disentangle the two scenarios of evolution of ecological specialization, we carried out a selection experiment with a flea, Xenopsylla ramesis, and two sympatric rodent hosts, Meriones crassus and Dipodillus dasyurus. Fleas (Insecta: Siphonaptera) are obligatory haematophagous parasites of higher vertebrates and are especially abundant and diverse in small mammals. They usually alternate between periods in which they occur on the body or in the burrow of their host. In most cases, pre-imaginal development of fleas takes place entirely off-host. The larvae are usually not parasitic, feeding on a variety of organic debris. In contrast to many other parasites, flea infestation on living hosts can be easily manipulated and monitored for changes in individual traits over time (e.g. Krasnov et al., 2004b). Both rodent hosts used in our study are naturally infested with X. ramesis (Krasnov et al., 1997, 1999), although D. dasyurus represents a somewhat inferior host than M. crassus (Krasnov et al., 2004b).

Numerous laboratory selection experiments with phytophagous arthropods (e.g. Gould, 1979; Fry, 1990a,b; Fry, 1992, Fry, 1999; Tucic et al., 1995; Agrawal, 2000; Magalhães et al., 2009; Messina et al., 2009) and microparasites (Ebert, 1998; Crill et al., 2000; Turner & Elena, 2000; Duffy et al., 2006; Little et al., 2006; Ferris et al., 2007; Schulte et al., 2011) aimed to investigate whether adaptation to one host influenced performance on alternative hosts. However, fewer experimental studies have been conducted with macroparasites (e.g. Jaenike & Dombeck, 1998; Davies et al., 2001; Paterson & Barber, 2007), and haematophagous arthropod parasites have been largely neglected, possibly due to the difficulty to maintain and manipulate these organisms under laboratory conditions. Moreover, for reasons related to the eradication of introduced pests and parasites, previous studies on host shifts had chiefly focused on the introduction of phytophages or parasites to totally novel hosts (e.g. Agrawal, 2000; Crill et al., 2000; Magalhães et al., 2009). However, the detection of functional trade-offs in such systems might be limited because these trade-offs are expected to be experimentally observable only in case of genetic equilibrium on two hosts (see Joshi & Thopmson, 1995 for detailed explanation).

Here, both host species were familiar to the fleas, but fleas were prevented from exploiting one of the hosts for several generations. Besides testing for lost performance on a foregone host, this design allowed evaluating whether the loss of ability to exploit a bygone host is related to (a) a trade-off between the costs of the exploitation of alternative hosts or (b) relaxed selection on adaptations associated with the exploitation of the unexploited host.

We maintained three replicate populations of fleas on each of the two hosts (hereafter referred to as two flea lines) for nine generations. In each generation, we examined the reproductive performance of fleas exploiting either their maintenance host or the alternative host. Accordingly, fleas maintained on M. crassus were transferred to D. dasyurus and vice versa. Specifically, we tested whether fleas maintained on a single host species for several generations (a) exhibited increased performance on their familiar host and (b) reduced their performance on an alternative host. Decreased performance on an alternative host with or without a concomitant increase in performance on its maintenance host would support the ‘trade-off’ scenario, whereas decreased performance on an alternative host without a concomitant increase in performance on its maintenance host would support the ‘relaxed selection’ scenario.

Materials and methods

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

Initial parasite population

The initial flea population was established from a colony of X. ramesis routinely maintained in our laboratory on both M. crassus and D. dasyurus. The colony started in 1999 from specimens collected in the field from both host species. Each rodent was kept in a plastic cage that contained a nest box, a screen floor and a pan containing a mixture of sand or loess soil and flea nutrient medium. Each host rodent was infested with 20–30 newly emerged fleas and gravid female fleas deposited their eggs in the substrate. Every 2 weeks, the substrate and bedding materials were removed from the cages into plastic boxes covered with perforated lids and transferred into an incubator (FOC225E, Velp Scientifica srl, Milano, Italy), where flea development and emergence took place at 25 °C and 75% relative humidity. For each new infestation, 30–50 fleas were chosen at random from parents maintained on the two host species and mixed. Every year, we added 100–150 field-captured fleas collected from both M. crassus and D. dasyurus to our colony by randomly distributing them among the hosts of either species. Further details regarding flea rearing and maintenance can be found elsewhere (Khokhlova et al., 2009, 2010).

Host animals

We used M. crassus and D. dasyurus from our laboratory colonies, established in 1997 (see details in Krasnov et al., 2004b). Rodents were maintained in 60 × 50 × 40 cm plastic cages at 25 °C with a photoperiod of 12:12 h and sawdust as bedding material. Rodents were offered millet seed and fresh alfalfa (Medicago sp.) ad libitum. No free water was provided as these rodents obtain all of their water from plants.

Experimental design

Six, c. 8-month-old adult males of each rodent species were used as hosts. Both M. crassus and D. dasyurus have been shown to acquire some level of resistance after repeated infestation by fleas (Khokhlova et al., 2004a,b). This resistance was shown to be nonspecific with regard to the identity of the source fleas, but rather to be equally effective against several flea species (i.e. cross-resistance; Khokhlova et al., 2004a,b). To ensure similar background levels of acquired resistance, hosts were subjected to standardized exposure to fleas. Two weeks prior to the onset of the experiment and at 2-day intervals, each host was exposed to 3–2-hour sessions of infestation by 10 male and 20 female X. ramesis. Following, we carried out serial transfers of flea populations on each of the two hosts. Three individuals of each host species were used for flea maintenance, that is, there were three replicates for each flea line. Three other individuals of each host species were used for testing the reproductive performance of fleas from both lines in each generation, that is, tests of performance of each generation were replicated three times.

Fleas of the initial (hereafter, parent) generation were randomly collected from the colony. Fleas were then randomly divided into six groups (10 males and 20 females each) and were randomly assigned to maintenance hosts. After fleas of the parent generation were placed on their hosts, they were allowed to feed on these hosts only and to lay eggs into the substrate of their cages. Two weeks later, all substrate and bedding materials were collected from the cages and the hair of the rodents was brushed until all fleas were recovered. Substrate and bedding materials from each cage were placed in individual plastic boxes and were transferred to an incubator. Ten days later, the plastic boxes were inspected once a day for 2 weeks, and all newly emerged fleas were collected.

Fleas that emerged in each plastic box, that is, ‘generation 1’ of each maintenance host, were randomly divided into three groups. One group was placed on a randomly selected maintenance host, that is, a host belonging to the same species as a host of its previous generation, and was the source of the following generation, that is generation 2. Fleas belonging to the two remaining groups were randomly introduced to either M. crassus or D. dasyurus test hosts, and their reproductive performance on these hosts was examined. These procedures were repeated for nine generations. In other words, we tested the reproductive performance of fleas of either M. crassus or D. dasyurus on both their maintenance host species and on an alternative host for each of nine generations. In total, we measured reproductive performance of 108 flea groups (two maintenance hosts × two alternative hosts × nine generations × three replicates).

Measurement of reproductive performance

Reproductive performance of fleas was estimated from (a) the mean number of eggs produced by a female flea, (b) flea pupation success and (c) flea emergence success. To obtain flea eggs, we used newly emerged fleas that were not allowed to feed from their emergence until their assignment to the experimental treatments. During the period between emergence and experimental exposure, these fleas were maintained in incubators at 25 °C and 75% RH. Each host was placed in a tightly fitted tube made of 5 × 5 mm mesh wire. The tubes were 15 cm long and 5 cm in diameter for M. crassus, and 10 cm long and 2 cm in diameter for D. dasyurus, which limited their movement and prevented self-grooming. Tubes with rodents were individually placed in white plastic tubs. A group of 20 female and 10 male fleas was placed on each host. After feeding on a host for 90 min, fleas were collected by brushing the host’s hair, using a tooth-brush, until all fleas were recovered. Fleas collected from each host were placed in a 50-ml glass vial, the bottom of which was covered with a thin layer of sand and small pieces of filter paper, and transferred into an incubator maintained at 25 °C and 92–95% relative humidity. Feeding procedure was repeated daily, for each group of fleas, on the same host individual for eight consecutive days. Every day, pieces of filter paper from each vial were examined thoroughly for eggs under a light microscope. The day of oviposition (counted from the first feeding) was recorded and eggs were counted. The first oviposition invariably occurred on the fourth day of feeding in all flea groups. The mean number of eggs produced per female flea during the 5 days following the first oviposition event was calculated for each flea group.

Eggs produced by each female group were placed in individual 20-ml glass vials, which contained a layer of 3-mm sand and larval food medium (94% dry bovine blood, 5% millet flour and 1% grinded excrements of a rodent host). The vials were covered by perforated lids and were maintained at 25 °C and 92% RH (see Krasnov et al., 2004b for further details). Starting from day 10 after the first oviposition event, each vial was monitored once a day, and the numbers of pupae and emerged adults were recorded. Vials were monitored until no additional adults emerged for 30 consecutive days. Pupation and emergence success were calculated for each flea group as the proportion of eggs that attained a pupa stage and the proportion of pupae that attained emergence, respectively.

Data analysis

Prior to analyses, the mean number of eggs produced per female flea was log-transformed, and pupation and emergence successes were angular-transformed to satisfy the assumptions of parametric statistics. These transformations produced distributions that did not significantly differ from normality (Kolmogorov–Smirnov tests, > 0.20 for all comparisons).

To test whether flea reproductive performance changed over generations on the maintenance and the alternative hosts, data were analysed using generalized linear models (GLM; separate slope design) with normal distribution and log-link functions. Separate analyses were carried out for flea lines maintained on M. crassus and D. dasyurus hosts. The dependent variables were the mean number of eggs produced by a female flea, and pupation and emergence success, that is, proportion of pre-imaginal fleas that attained pupation stage and proportion of pupae from which new adults emerged, respectively, with generation as a continuous factor and host species as a categorical factor. In addition, the effect of the number of generations in fleas maintained and tested on D. dasyurus (see Results) on the mean number of eggs per female flea was analysed using a nonlinear estimation of the breakpoint of piecewise linear regression (Bacon & Watts, 1971). Figures present the untransformed data.

Results

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

Egg production of fleas from both lines significantly varied between hosts (Wald statistics = 93.75 and 281.41 for the M. crassus and D. dasyurus lines, respectively; d.f. = 1, < 0.05 for both); however, this pattern was not consistent over generations (generation × host interaction; Wald statistics = 7.19 and 41.15 for the M. crassus and D. dasyurus lines, respectively; d.f. = 2, < 0.05 for both). Specifically, although GLM analysis did not detect a significant effect of generation on egg production of fleas maintained and tested on the same host, a significant gradual increase in egg production was detected, from generation 1 to generation 4, in fleas of the D. dasyurus line on their maintenance host (slope = 0.18 ± 0.06, t10 = 4.80, < 0.01), resulting in c. 55% greater egg production during generations 4–9, compared to generation 1 (Fig. 1b), with no further changes beyond generation 4 (slope = −0.01 ± 0.03, t13 = 0.50, = 0.63). In contrast, no changes in egg production were detected over generations in fleas of the M. crassus line on their maintenance host (Fig. 1c). When transferred to an alternative host, fleas of both lines significantly reduced their egg production by c. 65–75%, starting generation 6 (Table 1, Fig. 1).

image

Figure 1.  Mean (±1 SE) number of eggs produced during 5 days of oviposition by fleas maintained for nine generations on either Dipodillus dasyurus (a and b) or Meriones crassus (c and d) and exploited either M. crassus (a and c) or D. dasyurus (b and d).

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Table 1.   Coefficients of the generalized linear models (GLMs, separate slope design) testing for the effect of host species and number of generations on reproductive performance for fleas Xenopsylla ramesis maintained for nine generations on either Meriones crassus (Mc) or Dipodillus dasyurus (Dd) (maintenance hosts; MH) and exploited either M. crassus or D. dasyurus. Egg number is the mean number of eggs produced per female flea during 5 days of oviposition; pupation success is the proportion of eggs that attained pupation; and emergence success is the proportion of pupa that attained emergence.
MHReproductive variableHostCoefficient ± SEWald statisticsP
McEgg numberDd−0.11 ± 0.047.180.002
Mc0.002 ± 0.030.010.80
DdDd0.04 ± 0.032.170.15
Mc−0.16 ± 0.0339.360.001
McPupation successDd−0.08 ± 0.0126.350.005
Mc−0.002 ± 0.010.040.90
DdDd0.003 ± 0.010.090.89
Mc−0.07 ± 0.0128.980.001
McEmergence successDd−0.14 ± 0.0261.590.001
Mc−0.0002 ± 0.010.00040.98
DdDd−0.004 ± 0.010.090.77
Mc−0.14 ± 0.0167.620.001

In both flea lines, the effects of host identity on pupation success were significant (Wald statistics = 7.57 and 15.96, for the M. crassus and D. dasyurus lines, respectively; d.f. = 1, < 0.05 for both) but not consistent over generations (generation × host interaction; Wald statistics = 26.29 and 29.07, for the M. crassus and D. dasyurus lines, respectively; d.f. = 2, < 0.05 for both). A similar pattern was found for emergence success (host species: Wald statistics = 43.46, d.f. = 1 and 40.48, d.f. = 1, for the M. crassus and D. dasyurus lines, respectively; generation × host interaction: Wald statistics = 61.69, d.f. = 2 and 67.71, d.f. = 2 for the M. crassus and D. dasyurus lines, respectively; < 0.05 for all). In contrast to egg production, pupation and emergence success in fleas exploiting their maintenance host did not demonstrate significant changes over time (Table 1, Figs 2b, c and 3b, c). However, when transferred to alternative hosts, both pupation and emergence successes steadily and significantly decreased by c. 50%, starting at generations 3–5 (Table 1, Figs 2a, d and 3a, d).

image

Figure 2.  Mean (±1 SE) proportional pupation success of eggs produced by fleas maintained for nine generations on either Dipodillus dasyurus (a and b) or Meriones crassus (c and d) and exploited either M. crassus (a and c) or D. dasyurus (b and d).

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image

Figure 3.  Mean (±1 SE) proportional emergence success of pupae produced by fleas maintained for nine generations on either Dipodillus dasyurus (a and b) or Meriones crassus (c and d) and exploited either M. crassus (a and c) or D. dasyurus (b and d).

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Discussion

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

Fleas maintained on a single host species for a few generations substantially decreased their reproductive performance when transferred to an alternative host species, whereas they did not increase their performance on a maintenance host except for one of the three performance measures (number of eggs) in fleas of one of the two lines (the D. dasyurus). Therefore, the results primarily support the ‘relaxed selection’ hypothesis of the evolution of ecological specialization in haematophagous ectoparasites, suggesting that trade-offs alone are less likely to promote specialization in this system.

Deterioration of performance on an alternative host

Differential performance of generalist parasites in different host species (Krasnov et al., 2004b) requires the development of a wide spectrum of adaptations to cope with a wide range of host defences (Poulin, 1998). In particular, host’s immune responses may inhibit parasite feeding and/or reproduction (Fielden et al., 1992; Walker et al., 2003; but see Khokhlova et al., 2010) and promote an evolutionary arms race, whereby parasites develop counter-adaptations against the host’s defences (Combes, 1997; Lehane, 2005). It has been suggested, although yet to be proven, that the production of immunomodulators and additional adaptations related to host immunosuppression are costly (Combes, 1997). Accordingly, parasite traits that are targeting a specific host are expected to lose their adaptive value and deteriorate during periods in which that host is only rarely encountered or exploited (Poulin, 2007). Over evolutionary time scales, such deteriorations may occur due to relaxed selection related to direct costs of ‘obsolete adaptions’ (Lahti et al., 2009), which are followed by neutral mutational deterioration (Huxley, 1953; Estes et al., 2005; Roles & Conner, 2008). Evidence supporting relaxed selection as the driving force of the loss of ability to exploit an alternative host has been reported in phytophagous mites. Mites adapted to a novel host plant and then reverted to their original host plant rapidly lost their newly acquired adaptations to the novel host (Agrawal, 2000).

In our study, a swift and sharp decrease in flea reproductive performance was detected merely few generations after their transfer to an alternative host, which might imply the involvement of epigenetic modifications, that is, heritable changes in gene expression and function, which do not involve changes in DNA sequence (Richards, 2006). Moreover, if the exploitation of multiple hosts requires a wide spectrum of adaptations against multiple defence systems, then prolonged flea maintenance on a given host could be accompanied by both epigenetic activation of specific genes involved in coping with the host’s immune defences and epigenetic silencing of genes that are less relevant to flea performance on their maintenance hosts. The results suggest that the latter scenario might be more probable because no substantial improvement in performance was observed in fleas that were kept on their maintenance hosts, except for number of eggs in the D. dasyurus line. Alternatively, although not mutually exclusively, the initial flea population might have had sufficient levels of genetic variation in traits relevant to host defences, in which case the results might have reflected a true evolutionary changes (e.g. Via, 1990; Berlocher & Feder, 2002). However, further work is needed to explore the heritability of the studied traits and the potential roles of epigenetic and genetic processed underlying the observed results.

The main proximate reason for the lack of improvement in reproductive success when exploiting the maintenance hosts could be related to morphological and physiological constraints that determine species-specific reproductive output in fleas (Krasnov, 2008). Although clutch size depends on numerous intrinsic (e.g. age, nutrition status, host species) and extrinsic (e.g. ambient temperature, light regime) factors, it is mainly associated with the number of ovarioles that compose an ovary, which is relatively conservative within flea species and genera (Darskaya et al., 1965; Vashchenok, 1988). Therefore, it is possible that fleas, at least those of the M. crassus line, already attained their maximal fecundity and thus could not demonstrate further improvement following additional residence time on that host. Similar constraints may be also responsible for the lack of further increases in egg production in fleas of the D. dasyurus line on their maintenance hosts beyond generation 4 (Fig. 1b).

Differential flea responses to maintenance on the two hosts

Whereas fleas reared on D. dasyurus rapidly increased their egg production on their maintenance host, fleas maintained on M. crassus did not demonstrate any such increase in fitness over generations. In general, D. dasyurus had been shown to be an inferior host for X. ramesis compared to M. crassus (Krasnov et al., 2004a). Furthermore, egg production in fleas of the D. dasyurus line in generation 1 was lower on G. dasyurus than on M. crassus, although this was not the case in fleas of the M. crassus line. Increasing egg production in fleas of the D. dasyurus line on D. dasyurus suggested that the fleas were able to ‘fine-tune’ their exploitation of the maintenance host.

The contrasting changes over generations in egg production on the maintenance host between the two flea lines could have also resulted from ‘individual specialization’ (Bolnick et al., 2003; Aroujo et al., 2011). According to this concept, a population of a generalist species may comprise individuals with somewhat variable niches, which are subsets of the larger population niche. However, the mechanisms underlying individual specialization are not well established (see review in Aroujo et al., 2011). Regardless of its precise underlying causes and mechanisms, individual specialization might result in polymorphism in host preference within the same local parasite population. In our system, it is possible that some individual fleas in the parental population were better adapted to M. crassus, whereas others performed better on D. dasyurus. The somewhat higher performance of X. ramesis on M. crassus than on D. dasyurus (Krasnov et al., 2004b) suggests that these initial subpopulations might have differed in their relative abundances, with M. crassus-specialists being more abundant than D. dasyurus-specialists. It can thus be speculated that in the M. crassus line, the individuals specialized on D. dasyurus might have been rapidly selected against, while no changes occurred in individuals specializing on M. crassus. Similarly, in the D. dasyurus line, fleas that better performed on M. crassus were selected against, although such selection was expectedly slower, merely because subpopulation of M. crassus-specialists likely constituted the majority of the initial flea population.

An additional interpretation of the variable performance of the two flea lines on the maintenance hosts could be related to fact that the evolution of ecological specialization is context-dependent and thus might differ among host–parasite associations. For example, a bacteriophage adapted to a Salmonella host demonstrated decreased performance on Escherichia, whereas adaptation to Escherichia did not affect its performance on Salmonella (Crill et al., 2000). Further experiments with bacteriophages showed that (a) although expansion of the host range often imposed a cost on the standard laboratory host, it was not always the case (Duffy et al., 2006; Ferris et al., 2007) and (b) patterns of host range expansion could be asymmetric among host strains (Duffy et al., 2006). These studies and our findings demonstrate that patterns of host range expansion of the same parasite may depend on the identities and particularities of the available host species and are thus expected to vary geographically.

In conclusion, our findings suggest that ectoparasites may develop differential and asymmetrical host preferences, which are contingent on the history of their host associations. In addition, ectoparasite performance on their preferable hosts is strongly influenced by morphological and/or physiological constraints. Our results call for further investigation into the specific factors underlying the costs and benefits of prolonged association with specific hosts and its potential micro- and macroevolutionary implications.

Acknowledgments

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

We thank two anonymous referees for their extremely helpful comments on the earlier version of the manuscript. This study was supported by the Israel Science Foundation (Grant no. 27/08 to BRK and ISK). This is publication no. 762 of the Mitrani Department of Desert Ecology.

References

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

Data deposited at Dryad: doi: 10.5061/dryad.b37h81h1