Insect Science (2014) 21, 401–414, DOI 10.1111/1744-7917.12064

MINI REVIEW

Insect host–parasite coevolution in the light of experimental evolution Niels A. G. Kerstes and Oliver Y. Martin Experimental Ecology, Institute for Integrative Biology, D-USYS, ETH Zurich, Zurich, Switzerland

Abstract The many ways parasites can impact their host species have been the focus of intense study using a range of approaches. A particularly promising but under-used method in this context is experimental evolution, because it allows targeted manipulation of known populations exposed to contrasting conditions. The strong potential of applying this method to the study of insect hosts and their associated parasites is demonstrated by the few available long-term experiments where insects have been exposed to parasites. In this review, we summarize these studies, which have delivered valuable insights into the evolution of resistance in response to parasite pressure, the underlying mechanisms, as well as correlated genetic responses. We further assess findings from relevant artificial selection studies in the interrelated contexts of immunity, life history, and reproduction. In addition, we discuss a number of well-studied Tribolium castaneum–Nosema whitei coevolution experiments in more detail and provide suggestions for research. Specifically, we suggest that future experiments should also be performed using nonmodel hosts and should incorporate contrasting experimental conditions, such as population sizes or environments. Finally, we expect that adding a third partner, for example, a second parasite or symbiont, to a host–parasite system could strongly impact (co)evolutionary dynamics. Key words artificial selection, immunity, Nosema, reproduction, resistance, Tribolium

Introduction Experimental evolution can be defined as “the study of evolutionary changes occurring in experimental populations as a consequence of conditions imposed by the experimenter” (Kawecki et al., 2012). This approach has been shown to be highly valuable for studying a wide range of evolutionary questions including host–parasite conflict (Garland & Rose, 2009; Kawecki et al., 2012). To date, there have also been several experimental evolution studies investigating the evolution of resistance to focal parasites or pathogens in insect hosts.

Correspondence: Oliver Y. Martin, Experimental Ecology, Institute for Integrative Biology, D-USYS, ETH Zurich, Universit¨atsstrasse 16, CH-8092 Zurich, Switzerland. Tel: +41 44 632 36 60; fax: +41 44 632 12 71; email: [email protected]

There are essentially four types of experimental evolution studies that can lead to insights into host–parasite coevolutionary dynamics and underlying mechanisms. Experimenters could (1) track evolutionary changes in host populations that are exposed to: (i) noncoevolving parasites, (ii) select on particular immune traits directly, or (iii) assess immune traits as a correlated response to selection on other (e.g. reproductive) traits. Finally, in experimental host–parasite coevolution, both the hosts and the parasites are allowed to evolve and adapt to each other. There are only a few examples of long-term experimental coevolution studies performed using insect hosts. Long-term experiments involving the Indian meal moth (Plodia interpunctella) and its granulosis virus led to valuable insights into the effect of parasites on insect host population dynamics (Sait et al., 1994; Bjornstad et al., 1998; Knell et al., 1998), but no data were collected on the 401

 C 2013

Institute of Zoology, Chinese Academy of Sciences

402

N. A. G. Kerstes & O. Y. Martin

evolution of resistance or parasite virulence. Maintaining Drosophila melanogaster populations together with populations of the parasitoid Asobara tabida resulted in an increase in host resistance, while parasitoid virulence did not change. The increase in resistance was found to be traded off with larval competitive ability (Green et al., 2000). In other experiments, populations of the red flour beetle, Tribolium castaneum, were either maintained parasite-free or forced to coevolve with the microsporidian, intercellular parasite Nosema whitei. Because the Tribolium–Nosema system is particularly well studied, we discuss it in more detail (see Section “Experimental coevolution of T. castaneum and N. whitei”) to illustrate the relevance and the wide scope of such longterm coevolution studies.

Experimental evolution in the context of host–parasite conflict Experimental evolution studies are particularly well suited to the study of coevolutionary processes involving more than one species (reviewed in Brockhurst & Koskella, 2013). In the context of coevolution between insect hosts and their parasites, several studies have assessed how host resistance evolves using different approaches. A summary of the findings of selection studies where particular insect hosts have been exposed to noncoevolving parasites in the lab is given in Table 1. The most commonly observed result is an increase in host resistance, for example, via higher survival (Boots & Begon, 1993; Kraaijeveld & Godfray, 1997; Fellowes et al., 1998; Ye et al., 2009; Trienens & Rohlfs, 2011), or via improved immune response to parasite infection (Hughes & Sokolowski, 1996). Often, but not always, this increase in resistance is found to trade off with nonimmune traits, such as competitive ability (Kraaijeveld & Godfray, 1997) and development time (Boots & Begon, 1993). Basically, there are two explanations for such trade-offs between resistance against parasite infection and other fitness components. First, hosts have limited resources that they allocate to immune-related traits instead of to other functions such as development or reproduction (Webster & Woolhouse, 1999; Kraaijeveld et al., 2001; Cotter et al., 2004). Second, fitness benefits in one trait might be associated with fitness costs in another trait (i.e. antagonistic pleiotropy) (Kraaijeveld & Godfray, 1997). Antagonistic pleiotropy could occur when one gene has more than one function, for instance when a gene is involved in both the immune response as well as another nonimmune related trait. We also note that not all studies where researchers exposed focal hosts to pathogens have successfully lead to the evo C 2013

lution of increased resistance (Burges, 1971; Briese & Podgwaite, 1985; Lindfield, 1990; reviewed in Boots & Begon, 1993). Other studies with direct relevance to host–parasite interactions have focused more directly on insect host immunity and incorporated selection on particular immune traits (see Table 2), such as the key enzyme phenoloxidase (PO) (reviewed in Gonz´alez-Santoyo & Cord´oba-Aguilar, 2011). For instance, Schwarzenbach and colleagues used bidirectional artificial selection to select for high and low values of PO in the yellow dung fly, Scathophaga stercoraria (Schwarzenbach & Ward, 2006). Alternatively, immune measures could be assessed as a correlated response to selection on other, for example, life history (Koella & Agnew, 1999; Koella & Offenberg, 1999; Koella & Bo¨ete, 2002; Pijpe et al., 2006), cuticular color (Armitage & Siva-Jothy, 2005; Cotter et al., 2008), or reproductive traits (Hosken, 2001; Hosken et al., 2001; Hosken & Ward, 2001; Martin et al., 2004). There are now numerous selection studies using insect models where investment in reproduction in both sexes has been selected by varying the intensity of sexual selection and sexual conflict, especially focusing on speciation (Hosken et al., 2009). This has been achieved via selection regimes incorporating monogamy versus polyandry (e.g. Hosken et al., 2001; Demont et al., 2013), contrasting sex ratios (e.g. Ingleby et al., 2010; Michalczyk et al., 2011a), different population densities (Martin & Hosken, 2003a, b, 2004), or life history schedules (Maklakov et al., 2009, 2010). Generally, the output from other selection experiments in this context has not included assays of immune measures or resistance to parasites. However, there has been some work on this topic on S. stercoraria (Hosken, 2001; discussed in Gonz´alez-Santoyo & Cord´oba-Aguilar, 2011), P. interpunctella (McNamara et al., 2013), and T. castaneum (Hangartner et al., 2013). Hosken assessed PO activity of males and females of monogamous and polyandrous selection lines and found that polyandrous individuals had decreased PO, suggesting that investment in reproductive tissue came at a cost to immunity (see Table 2). This provides an emphatic experimental illustration of the intimate connections between immunity and reproduction (see, e.g. Siva-Jothy et al., 1998; Rolff & Siva-Jothy, 2002). In P. interpunctella, immunity also responded to differences in sexual selection intensity during experimental evolution, with males from female-biased populations having lower PO (but not antibacterial lytic activity, highlighting how different immune components may respond differently) (McNamara et al., 2013). In contrast, in T. castaneum there was no evidence of differences in immune investment (assessed via PO and resistance to natural Nosema parasite; Hangartner et al., 2013), despite clear Institute of Zoology, Chinese Academy of Sciences, 21, 401–414

 C 2013

Drosophila melanogaster (Diptera: Drosophilidae)

Host species

Selection regimes

Institute of Zoology, Chinese Academy of Sciences, 21, 401–414 5

5

5

S: four selection lines selected for increased resistance via exposure to parasitoid attack UC: four lines not exposed to parasitoid Selection lines described above Selection lines described above

Endoparasitoid Leptopilina boulardi (Hymenoptera: Eucoilidae)

Drosophila host versus A. tabida and L. boulardi Drosophila host versus A. tabida and L. boulardi

In S lines from the two selection experiments outlined above, decreased competitive ability was associated with reduced larval feeding rates S flies have ca. twice as many haemocytes than UC

No cross-resistance or trade-offs in resistance of S when tested for resistance against fungus Beauveria bassiana or microsporidian Tubulinosema kingi (Microsporidia: Tubulinosematidae) Increased resistance: ca. 45% of S flies survive attack versus ca. 0.4% in UC Correlated response: S flies suffer from lower larval survival under moderate-to-severe intraspecific competition; no significant differences in fecundity, egg viability (hatch rates), or adult starvation tolerance

5

5

Selection lines described above Selection lines described above

Higher frequency of encapsulation in larvae from populations exposed to wasps No change in larval foraging behavior (i.e. proportion of rover versus sitter; rover larvae are more easily detected by the parasitoid) Increased resistance: host survival increases from 5% in UC to 60% in S Correlated response: reduced larval competitive ability under high competition. No significant differences in larval or pupal survival or development time, adult starvation tolerance, fecundity, adult size, or fluctuating asymmetry S males achieved greater mating success

19

5

Findings

Generations (host)

S: four lines selected for increased resistance UC: four lines not exposed to parasitoid

Parasitoid wasp Asobara S: three populations with wasps tabida (Hymenoptera: UC: three populations Braconidae) without wasps

Parasite/pathogen

(to be continued)

Cotter et al., 2004

Fellowes et al., 1999

Fellowes et al., 1998

Rolff & Kraaijeveld, 2003 Kraaijeveld et al., 2012

Kraaijeveld & Godfray, 1997

Hughes & Sokolowski, 1996

Reference

Table 1 Experimental evolution studies investigating evolution of resistance (as defined per study) to parasites or pathogens in insects. The table includes studies incorporating contrasting selection regimes where the host species was either exposed to the parasite/pathogen (selected lines: S) or maintained as unexposed control lines (UC).

Experimental host–parasite coevolution 403

Plodia interpunctella (Lepidoptera: Pyralidae)

Host species

Table 1 Continued.

 C 2013

S: three selected lines (injected with B. cereus spores) UC: control lines (CP: no infection, control puncture & CN: no infection, no puncture) S: three selected insect populations UC: three virus-free control populations 2 years

24

S: three selected lines UC: three lines not exposed to pathogen

Opportunistic bacterial pathogen Pseudomonas aeruginosa (Pseudomonadales: Pseudomonadaceae) Opportunistic bacterial pathogen Bacillus cereus (Bacillales: Bacillaceae)

Granulosis virus

10 + 15 (after five generations with no selection)

S: three lines where larvae were exposed to fungus UC: three fungus-free lines

26

Increased resistance: S moths were ca. twice as resistant to infection (LD50 s) as UC Correlated responses: longer development time, reduced egg viability, increased pupal weight in S

Flies from S did not have greater lifetime reproductive success than UC after infection. In the absence of infection S have lower reproductive success than UC Late-life fecundity was increased in S, whereas early-life fitness was inferior No cross-resistance or trade-offs in resistance of S when tested for resistance against parasitoid A. tabida Increased resistance: S less susceptible to A. nidulans mycotoxin Sterigmatocystin S larvae had higher survival rates in the presence of parasite than UC Evolved protection-specific, as S not better at coping with other bacteria/mycotoxins Increased resistance: population-level survivorship 70% in S versus 15% in UC Cost of evolved increased defence = reduced longevity and larval viability Rapid loss of trait after five generations of relaxed selection Increased resistance: S flies required increased concentration of spores in order to cause 50% mortality Correlated responses: findings concerning some traits indicate evolution of resistance could come at a cost

15

S: three selection lines selected for increased tolerance UC: three lines not exposed to fungus Selection lines described above

Findings

Generations (host)

Selection regimes

Fungus Aspergillus nidulans (Eurotiales: Trichocomaceae)

Fungus B. bassiana (Hypocreales: Clavicipitaceae)

Parasite/pathogen

Boots & Begon, 1993

Ma et al., 2012

Ye et al., 2009

Trienens & Rohlfs, 2011

Kraaijeveld et al., 2012

Kraaijeveld & Godfray, 2008

Reference

404 N. A. G. Kerstes & O. Y. Martin

Institute of Zoology, Chinese Academy of Sciences, 21, 401–414

 C 2013

Trait

Life history Aedes aegypti (Diptera: Culicidae)

Pupation time

Immunity Scathophaga Phenoloxidase (PO) stercoraria activity (Diptera: Scathophagidae)

Species

0, 2 & 4

15

see above; lines tested versus two pathogens (entomopathogenic fungus Metarizium anisopliae [Hypocreales: Clavicipitaceae], parasitic mite Pediculoides mesembrinae [Phthiraptera: Menoponidae]) Two selection regimes, each with three replicate lines: early pupation (EP) versus late pupation (LP)

15

Generations (host)

Three selection regimes, each with three replicate lines low PO (L) high PO (H) unselected control (UC)

Selection regimes

Reference

Institute of Zoology, Chinese Academy of Sciences, 21, 401–414 (to be continued)

Larvae exposed to low and high concentration Koella & Agnew, 1999 of spores of microsporidian parasite Edhazardia aedis (Microspora: Culicosporidae): after four generations mortality was higher in LP than in EP Correlated response of virulence and mode of transmission of E. aedis to selection on host pupation age When EP mosquitoes died, they harbored mostly binucleate spores (i.e. responsible for vertical transmission) In contrast, LP mosquitoes were more likely to harbor uninucleate spores (responsible for horizontal transmission) Suggests that genetic basis host pupation age at pupation shapes parasite transmission mode

Selection successful: significantly different Schwarzenbach & PO levels Ward, 2006 Correlated response in reproductive/fitness traits: no negative genetic correlations between PO and reproduction. H had larger first clutches, and L flies had smaller clutches. However, H died earlier than L flies under starvation, indicating a survival cost of running at high PO in the absence of challenge Both pathogens had a negative impact on Schwarzenbach & longevity, but selection regime flies did not Ward, 2007 differ in resistance to pathogens So, PO level is not a good predictor for overall resistance H flies did not live longer under starvation than L flies

Findings

Table 2 Studies in insects directly incorporating artificial selection on particular immune traits or incorporating selection pressures associated with relevant contexts (selection on life history or cuticular colour; experimental evolution targeting reproduction).

Experimental host–parasite coevolution 405

 C 2013

Reproduction S. stercoraria (Diptera: Scathophagidae)

Spodoptera littoralis (Lepidoptera: Noctuidae)

Cuticular color Tenebrio molitor (Coleoptera: Tenebrionidae)

Species

Table 2 Continued.

Presence/ absence of sexual selection

Melanism

Color

Trait

Two selection regimes, each with four replicate lines: polyandry (P) versus monogamy (Mo) Selection lines described above

12

10

16

≥6

Koella & Bo¨ete, 2002

Koella & Offenberg, 1999

Reference

Institute of Zoology, Chinese Academy of Sciences, 21, 401–414

(to be continued)

Hosken et al., 2001; P flies invested more in reproductive tissue Hosken & Ward (increased size of P female accessory 2001 glands, larger testes in P males). Investment influenced paternity in sperm competition. P flies have reduced immune function. Greater Hosken, 2001 investment in reproductive traits (see above) in P males and females came at a cost to immunity

M had lower PO activity and higher lysozyme Cotter et al., 2008 activity than N. Evidence for genetic trade-offs between the two immune responses (PO and lysozyme activity), and also between PO activity and melanism. Investment in PO is costly: lines with high PO activity had slower development rates

Correlated responses to selection on body Armitage & color: both hemocyte density and Siva-Jothy, 2005 pre-immune challenge PO activity were significantly higher in B compared to T lines

Age at pupation differs by ca. 0.7 d Associated increased wing length of LP mosquitos Immune measure = ability to encapsulate + melanize Sephadex bead: only 6% of EP mosquitoes strongly or completely melanized the bead, versus 32% of LP. Suggests genetic correlation between pupation age and immunity

10

Two selection regimes, each with 10 replicate lines each tan (T) black (B) (NB in this and other species, darker individuals are more resistant to pathogens) Two dark/melanic (M) versus two pale/nonmelanic (N) lines versus one control

Assays of correlated responses in life history traits adult size, fecundity, pre-adult survival across range of environments

7

Selection line mosquitos (see above) exposed to six environments (three food levels × two E. aedis infection levels) Selection lines described above

Findings

Generations (host)

Selection regimes

406 N. A. G. Kerstes & O. Y. Martin

 C 2013

Institute of Zoology, Chinese Academy of Sciences, 21, 401–414 Three selection regimes, each with three replicate lines: Male-biased sex ratio (MB) versus equal sex ratio (ESR) versus female-biased sex ratio (FB) Selection lines described above

Intensity of sexual selection (via sex ratio)

Tribolium castaneum (Coleoptera: Tenebrionidae)

10 and 12

Selection lines described above

Selected lines assessed for PO activity and Hangartner et al., 2013 host resistance to Nosema whitei (Microsporidia: Nosematidae), but no effect of selection

20

56

Ingleby et al., 2010

Martin et al., 2004

Reference

Males from FB populations lower PO activity McNamara et al., 2013 than ESR or MB males. No divergence in antibacterial lytic activity In male-biased selection lines, that is, those Michalczyk et al., experiencing high sexual selection, males 2011a have evolved to be superior competitors for reproductive success, while females have become more resistant to multiple mating

P females have lower reproductive success than Mo when mating once: P died earlier and produced fewer eggs + offspring MB females mate more frequently MB males invest more sperm per mating FB males mate three times more frequently than MB

Findings

ca. 80

ca. 55–60

Generations (host)

Selection regimes

Three selection regimes, each with three replicate lines: Male-biased sex ratio (MB) versus equal sex ratio (ESR) versus female-biased sex ratio (FB) Selection lines described above

Trait

Plodia interpunctella Intensity of sexual (Lepidoptera: selection (via sex Pyralidae) ratio)

Species

Table 2 Continued.

Experimental host–parasite coevolution 407

408

N. A. G. Kerstes & O. Y. Martin

divergence in reproductive investment in response to selection (Michalczyk et al., 2011a). Overall, in addition to assessments of evolved responses focusing on resistance to the focal parasite or pathogen or host immunity (see Tables 1 and 2), selection lines from the experiments outlined earlier have yielded a wealth of information concerning correlated responses (i.e. tradeoffs with life-history traits; see Tables 1 and 2 for details).

Experimental coevolution of T. castaneum and N. whitei Due to its convenient size, short generation time, and ease of maintenance and manipulation, T. castaneum has been used as a model organism by a wide range of researchers in various fields (Sokoloff, 1974; Klingler, 2004; Michalczyk et al., 2011b; Sbilordo et al., 2011; Grazer & Martin, 2012). T. castaneum has also been the subject of experimental evolution in a number of contexts (e.g. Michalczyk et al., 2011a; Tigreros & Lewis, 2011). In addition, the beetle’s genome has been sequenced (The Tribolium Genome Sequencing Consortium, 2008), and a variety of genetic tools are readily available, for example, genetic markers (Demuth et al., 2007) and RNA interference (Bucher et al., 2002). Furthermore, the beetle’s immune system has been studied in detail (Zou et al., 2007; Altincicek et al., 2008). Populations of T. castaneum harbor a wide range of parasites (Sokoloff, 1974), including N. whitei, which was found to be relatively common in natural populations (Burges & Weiser, 1973). N. whitei only infects young T. castaneum larvae (Blaser & SchmidHempel, 2005). Transmission of the parasite occurs after host death. Spores, which are formed in the host via clonal reproduction (Ironside, 2007), disperse in the environment and are ingested by new hosts, or new hosts acquire infections by cannibalizing on infected corpses. Infected individuals usually die during the late larval or pupal stages (Blaser & Schmid-Hempel, 2005). Those infected individuals that survive to adulthood suffer from decreased fitness, such as via reduced mating rates or reduced fecundity (Armstrong & Bass, 1986). Coevolution between T. castaneum and N. whitei has been studied in a number of independent, multigenerational experiments (Fischer & Schmid-Hempel, 2005; B´er´enos et al., 2009; Greef & Schmid-Hempel, 2010; see Table 3). Major points of interest were the role of genetic variation and the evolution of adaptive traits, such as host resistance and parasite virulence, during antagonistic coevolution. In addition, the Tribolium–Nosema system meets important assumptions of the Red Queen Hypothesis (Jaenike, 1978; Hamilton, 1980), one of the leading  C 2013

hypotheses for the evolution and maintenance of sex and recombination. The Red Queen Hypothesis proposes that parasites adapt to the most common host genotypes in a population (negative frequency-dependent selection). Sex and recombination via crossovers then constantly create rare host genotypes that are relatively fit. As N. whitei is an obligately killing parasite (Blaser & Schmid-Hempel, 2005), selection is strong on both antagonists. Strong selection on the parasite can theoretically favor higher recombination rates in the host under Red Queen dynamics (Salathe et al., 2008). Furthermore, there is a substantial epistatic component to resistance of T. castaneum against infection by N. whitei (Wegner et al., 2008; Wegner et al., 2009), and host genotype by parasite genotype interactions may be present (Otti, 2007; Kerstes & Wegner, unpublished data). Therefore, Tribolium–Nosema coevolution experiments have been used to test predictions based on the Red Queen Hypothesis. Results from these studies have led to important insights into the dynamics of host–parasite coevolution. For instance, it was shown that coevolution with N. whitei maintains elevated levels of host neutral genetic diversity and heterozygosity (B´er´enos et al., 2011b), thus supporting a more than 60-year-old hypothesis put forward by Haldane (1949). In addition to the maintenance of genetic variation, host resistance was found to have increased during coevolution (B´er´enos et al., 2009). Coevolved beetles from the same experiment were shown to have higher recombination frequencies than paired, noncoevolved beetles (Kerstes et al., 2012), which confirmed findings from an earlier Tribolium–Nosema coevolution study (Fischer & Schmid-Hempel, 2005), and which matches expectations based on a Red Queen scenario (Salathe et al., 2008). Moreover, the maintenance of genetic variation in coevolved beetle populations suggests the presence of negative frequency-dependent selection exerted by the parasite, especially since it was found that the maintenance of variation and high levels of heterozygosity could not be explained by a heterozygote advantage (Kerstes & Wegner, 2011). Alternatively, the maintenance of variation resulted from antagonistic pleiotropy, as it was shown that resistance against N. whitei is associated with costs in other traits (B´er´enos et al., unpublished data). Overall, the Tribolium–Nosema system has proven to be an excellent model system for investigating the dynamics of host–parasite coevolution. Yet, it proves to be hard to pinpoint the exact mechanisms behind all observations, possibly also because of the complex nature of the genetic architecture of T. castaneum resistance against N. whitei infection (Wegner et al., 2008). Furthermore, many aspects of the biology of the host appear to be influenced by the coevolving parasites (e.g. mating behavior), and Institute of Zoology, Chinese Academy of Sciences, 21, 401–414

Experimental host–parasite coevolution

409

Table 3 Overview of relevant findings from studies focusing on the Tribolium castaneum versus Nosema whitei system, including outputs from coevolution experiments and associated studies. Finding

Reference

Coevolution experiments In two of three independent coevolution experiments, coevolved beetles were found to have higher recombination frequencies than noncoevolved beetles T. castaneum resistance to infection by N. whitei increased during coevolution Coevolved beetles maintained higher genetic diversity, and heterozygosity, than paired, noncoevolved beetles Parasite-induced host mortality decreased during coevolution Coevolution did not lead to clear patterns of local adaptation Coevolution with N. whitei led to greater reproductive isolation between T. castaneum lines Mating rates of T. castaneum lines were influenced by both coevolving parasites and population size Additional experiments N. whitei is an obligately killing parasite that infects young T. castaneum larvae The fitness landscape of resistance of T. castaneum to infection with N. whitei is rugged and multipeaked, with peaks and valleys determined by epistatic interactions When focusing on the genetic architecture of T. casteneum resistance, different components play decisive roles in the host–parasite interactions when comparing single strain N. whitei infections to multiple strain N. whitei infections Heterozygosity is not a principal determinant of the T. castaneum resistance to infection by N. whitei

the effect of the parasites might interact with and depend on other environmental conditions (e.g. population size: Kerstes et al., 2013). It is clear that, even under controlled conditions, coevolutionary dynamics can be complex, and are unlikely to precisely match predictions based on simple models (e.g. the Red Queen model). Conclusions and future directions The Tribolium–Nosema experiments discussed earlier illustrate the considerable potential of experimental host–parasite coevolution performed with insect hosts. Inherently, such experiments are characterized by a high workload due to design and maintenance of the selection lines. Furthermore, immediate results will often be lacking, at least while coevolution is left to act for a number of generations. Nevertheless, in the longer term, experimental coevolution can be highly rewarding as it allows the targeted investigation of a myriad of open research questions. Findings from the Tribolium–Nosema system indicate that the outcome of host–parasite coevolution might depend on many aspects of the biology of both antagonists, such as

 C 2013

Fischer & Schmid-Hempel, 2005; Greef & Schmid-Hempel, 2010; Kerstes et al., 2012 B´er´enos et al., 2009 B´er´enos et al., 2011b B´er´enos et al., 2011a B´er´enos et al., 2012a B´er´enos et al., 2012b Kerstes et al., 2013

Blaser & Schmid-Hempel, 2005 Wegner et al., 2008

Wegner et al., 2009

Kerstes & Wegner, 2011

the mode of reproduction, or experimental conditions such as population size or the genetic diversity at the start of the experiment. Future studies would greatly benefit from closely following population genetic parameters, such as linkage disequilibrium and genetic diversity, over time. It would be particularly important that this is done in both antagonists, that is, hosts and parasites, as genotypic (and phenotypic) responses to coevolution are expected in both (Schulte et al., 2010). Experimental coevolution studies using insect hosts that also track the parasite’s evolutionary response are very rare, but essential for understanding host–parasite coevolutionary dynamics. Overall, the field would greatly benefit from additional host–parasite coevolution experiments, performed with a wider range of different hosts, parasites, and experimental conditions. There is also plenty of unfulfilled potential concerning associations between investment in resistance or immunity and reproduction, considering how closely linked these are (reviewed in Lawniczak et al., 2007; Scharf et al., 2013). This abundance of unanswered questions could be addressed in a targeted fashion by assessing immune traits in selection lines where there has been

Institute of Zoology, Chinese Academy of Sciences, 21, 401–414

410

N. A. G. Kerstes & O. Y. Martin

selection for altered reproductive investment. Overall, as outlined earlier, there have been a number of studies applying experimental evolution in this context, or artificial selection on reproductive traits, in a range of insect taxa: Coleoptera (e.g. Simmons & Garcia-Gonzalez, 2008; Maklakov et al., 2009; Michalczyk et al., 2011a; Katsuki et al., 2012), Diptera (e.g. Hosken et al., 2001; Miller & Pitnick, 2002; Martin & Hosken, 2003a, b; Wigby & Chapman, 2004), Lepidoptera (e.g. Fischer et al., 2006b, b, 2009), or Orthoptera (e.g. Morrow & Gage, 2001). These represent valuable resources and have been instrumental in furthering our understanding of reproduction in both sexes. Evolutionary responses in terms of immunity or parasite resistance in these lines, however, remain largely unexplored (see Hosken, 2001; Hangartner et al., 2013; McNamara et al., 2013 for exceptions). There are also a number of studies applying selection to lifespan (e.g. Wit et al., 2013), and here again close relationships with reproduction and immunity are expected. The considerable potential of selection lines in these contexts could be exploited, though, especially where lines are still running (or samples are available, depending on immune trait to be targeted). This approach would also work from the opposite direction, by utilizing selection lines exposed to increased parasite pressure or selected for immune performance to investigate correlated changes in reproductive traits (see Schwarzenbach & Ward, 2007). The majority of studies to date have focused on traditional laboratory workhorses such as Drosophila or Tribolium, so it would be valuable to have additional data from systems with closer connections to the situation in the field. In addition, it would also be worthwhile to incorporate a third coevolutionary player, for example, a second parasite, especially as multiple infections are expected to strongly influence the evolution of virulence (van Baalen & Sabelis, 1995), and consequently host–parasite dynamics. In this context, the impact of symbionts on host– parasite (co)evolutionary dynamics represents a largely unexplored research focus. In pea aphids (Acyrthosiphon pisum), for example, resistance against the aphid parasitoid Aphidius ervi is enhanced by the facultative symbiont Hamiltonella defensa (Dion et al., 2011). Furthermore, parasitoids exposed to highly resistant aphids harboring the symbiont were found to gain virulence over time (Dion et al., 2011). Further demonstration that symbionts can have a major influence on insect resistance, is provided by recent work on bumble bees (Bombus terrestris), where gut microbiota were found to protect individuals against infection by the trypanosomatid gut parasite Crithidia bombi (Koch & Schmid-Hempel, 2011). Interesting contrasting experimental conditions that would enable a more complete investigation of immu C 2013

nity (and reproduction) could include incorporation of a range of effective population sizes or different environments. Insect study species are often characterized by convenient husbandry and also ease of manipulation concerning external environments (e.g. via temperature or humidity of climate chambers), so such additional treatments would be eminently feasible. Resistance is strongly dependent on environmental variation (see Lazzaro & Little, 2009), as well as host (de Roode et al., 2004; Hughes & Boomsma, 2006; Ganz & Ebert, 2010) and parasite (Thompson & Lymbery, 1996) genetic diversity. A recent selection experiment performed with the mosquito Anopheles stephensi and the parasite Plasmodium gallinaceum confirms that host susceptibility to infection is indeed dependent on host genetics, parasite genetics, as well as the environment (Hume et al., 2011). The methods described in Hume et al. (2011) could serve as a guide for future host–parasite experimental evolution studies that simultaneously assess these complex factors in a targeted fashion.

Acknowledgments The authors thank Camillo B´er´enos and Sonja Sbilordo for comments, the Swiss National Science Foundation (SNF) for support (Ambizione grants PZ00P3-121777, PZ00P3137514, standard research grant 31003A_125144/1 to O. Y. Martin; N. A. G. Kerstes was supported by SNF grant 31003A_120451 to K. Mathias Wegner), and the Experimental Ecology group at ETH Z¨urich for being such excellent hosts.

Disclosure The authors declared that they have no conflict of interests.

References Altincicek, B., Knorr, E. and Vilcinskas, A. (2008) Beetle immunity: identification of immune-inducible genes from the model insect Tribolium castaneum. Developmental and Comparative Immunology, 32, 585–595. Armitage, S.A. and Siva-Jothy, M.T. (2005) Immune function responds to selection for cuticular colour in Tenebrio molitor. Heredity, 94, 650–656. Armstrong, E. and Bass, L.K. (1986) Effects of infection by Nosema whitei on the mating frequency and fecundity of Tribolium castaneum. Journal of Invertebrate Pathology, 47, 310–316.

Institute of Zoology, Chinese Academy of Sciences, 21, 401–414

Experimental host–parasite coevolution B´er´enos, C., Schmid-Hempel, P. and Wegner, K.M. (2009) Evolution of host resistance and trade-offs between virulence and transmission potential in an obligately killing parasite. Journal of Evolutionary Biology, 22, 2049–2056. B´er´enos, C., Schmid-Hempel, P. and Wegner, K.M. (2011a) Experimental coevolution leads to a decrease in parasite-induced host mortality. Journal of Evolutionary Biology, 24, 1777– 1782. B´er´enos, C., Schmid-Hempel, P. and Wegner, K.M. (2012a) Complex adaptive responses during antagonistic coevolution between Tribolium castaneum and its natural parasite Nosema whitei revealed by multiple fitness components. BMC Evolutionary Biology, 12: 11. B´er´enos, C., Schmid-Hempel, P. and Wegner, K.M. (2012b) Antagonistic coevolution accelerates the evolution of reproductive isolation in Tribolium castaneum. American Naturalist, 180, 520–528. B´er´enos, C., Wegner, K.M. and Schmid-Hempel, P. (2011b) Antagonistic coevolution with parasites maintains host genetic diversity: an experimental test. Proceedings of the Royal Society of London B (Biological Sciences), 278, 218–224. Bjornstad, O.N., Begon, M., Stenseth, N.C., Falck, W., Sait, S.M. and Thompson, D.J. (1998) Population dynamics of the Indian meal moth: demographic stochasticity and delayed regulatory mechanisms. Journal of Animal Ecology, 67, 110–126. Blaser, M. and Schmid-Hempel, P. (2005) Determinants of virulence for the parasite Nosema whitei in its host Tribolium castaneum. Journal of Invertebrate Pathology, 89, 251–257. Boots, M. and Begon, M. (1993) Trade-offs with resistance to a granulosis virus in the Indian meal moth, examined by a laboratory evolution experiment. Functional Ecology, 7, 528–534. Briese, D.T. and Podgwaite, J.D. (1985) Development of viral resistance in insect populations. Viral Insecticides for Biological Control (eds. K. Maramorosch & K.E. Sherman), pp. 361–398. Academic Press, New York. Brockhurst, M.A. and Koskella, B. (2013) Experimental coevolution of species interactions. Trends in Ecology and Evolution, 28, 367–375. Bucher, G., Scholten, J. and Klingler, M. (2002) Parental RNAi in Tribolium (Coleoptera). Current Biology, 12, R85–R86. Burges, H.D. (1971) Possibilities of pest resistance to microbial control agents. Microbial Control of Insects and Mites (eds. H.D. Burges & N.W. Hussey), pp. 445–457. Academic Press, London. Burges, H.D. and Weiser, J. (1973) Occurrence of pathogens of the flour beetle, Tribolium castaneum. Journal of Invertebrate Pathology, 22, 464–466. Cotter, S.C., Kruuk, L.E.B. and Wilson, K. (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. Journal of Evolutionary Biology, 17, 421–429.

 C 2013

411

Cotter, S.C., Myatt, J.P., Benskin, C.M.H. and Wilson, K. (2008) Selection for cuticular melanism reveals immune function and life-history trade-offs in Spodoptera littoralis. Journal of Evolutionary Biology, 21, 1744–1754. Demont, M., Grazer, V.M., Michalczyk, L., Millard, A.L., Sbilordo, S.H., Emerson, B.C., Gage, M.J.G. and Martin, O.Y. (2013) Experimental removal of sexual selection reveals adaptations to polyandry in both sexes. Evolutionary Biology, DOI: 10.1007/s11692-013-9246-3 (in press). Demuth, J.P., Drury, D.W., Peters, M.L., Van Dyken, J.D., Priest, N.K. and Wade, M.J. (2007) Genome-wide survey of Tribolium castaneum microsatellites and description of 509 polymorphic markers. Molecular Ecology Notes, 7, 1189– 1195. de Roode, J.C., Culleton, R., Cheesman, S.J., Carter, R. and Read, A.F. (2004) Host heterogeneity is a determinant of competitive exclusion or coexistence in genetically diverse malaria infections. Proceedings of the Royal Society of London B (Biological Sciences), 271, 1073–1080. Dion, E., Z´el´e, F., Simon, J.C. and Outreman, Y. (2011) Rapid evolution of parasitoids when faced with the symbiontmediated resistance of their hosts. Journal of Evolutionary Biology, 24, 741–750. Fellowes, M.D.E., Kraaijeveld, A.R. and Godfray, H.C.J. (1998) Trade-off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster. Proceedings of the Royal Society of London B (Biological Sciences), 265, 1553–1558. Fellowes, M.D.E., Kraaijeveld, A.R. and Godfray, H.C.J. (1999) Association between feeding rate and parasitoid resistance in Drosophila melanogaster. Evolution, 53, 1302–1305. Fischer, K., Bauerfeind, S.S. and Fiedler, K. (2006a) Temperature-mediated plasticity in egg and body size in egg size-selected lines of a butterfly. Journal of Thermal Biology, 31, 347–355. Fischer, K., Bot, A.N.M., Brakefield, P.M. and Zwaan, B.J. (2006b) Do mothers producing large offspring have to sacrifice fecundity? Journal of Evolutionary Biology, 19, 380– 391. Fischer, O. and Schmid-Hempel, P. (2005) Selection by parasites may increase host recombination frequency. Biology Letters, 1, 193–195. Fischer, K., Zimmer, K. and Wedell, N. (2009) Correlated responses to selection on female egg size in male reproductive traits in a butterfly. Evolutionary Ecology, 23, 389– 402. Ganz, H.H. and Ebert, D. (2010) Benefits of host genetic diversity for resistance to infection depend on parasite diversity. Ecology, 91, 1263–1268. Garland, T. and Rose, M.R. (2009) Experimental Evolution: Concepts, Methods, and Applications of Selection Experiments. University of California Press, Berkeley.

Institute of Zoology, Chinese Academy of Sciences, 21, 401–414

412

N. A. G. Kerstes & O. Y. Martin

Gonz´alez-Santoyo, I. and Cord´oba-Aguilar, A. (2011) Phenoloxidase: a key component of the insect immune system. Entomologia Experimentalis et Applicata, 142, 1–16. Grazer, V.M. and Martin, O.Y. (2012) Elevated temperature changes female costs and benefits of reproduction. Evolutionary Ecology, 26, 625–637. Greeff, M. and Schmid-Hempel, P. (2010) Influence of coevolution with a parasite, Nosema whitei, and population size on recombination rates and fitness in the red flour beetle, Tribolium castaneum. Genetica, 138, 737–744. Green, D.M., Kraaijeveld, A.R. and Godfray, H.C.J. (2000) Evolutionary interactions between Drosophila melanogaster and its parasitoid Asobara tabida. Heredity, 85, 450– 458. Haldane, J.B.S. (1949) Disease and evolution. La Ricerca Scientifica, 19, 68–76. Hamilton, W.D. (1980) Sex versus non-sex versus parasite. Oikos, 35, 282–290. Hangartner, S., Sbilordo, S.H., Michalczyk, L., Gage, M.J.G. and Martin, O.Y. (2013) Are there genetic trade-offs between immune and reproductive investments in Tribolium castaneum? Infection, Genetics and Evolution, 19, 45–50. Hosken, D.J. (2001) Sex and death: microevolutionary trade-offs between reproductive and immune investment in dung flies. Current Biology, 11, R379–R380. Hosken, D.J., Garner, T.W.J. and Ward, P.I. (2001) Sexual conflict selects for male and female characters. Current Biology, 11, 489–493. Hosken, D.J., Martin, O.Y., Wigby, S., Chapman, T. and Hodgson, D.J. (2009) Sexual conflict and reproductive isolation in flies. Biology Letters, 5, 697–699. Hosken, D.J. and Ward, P.I. (2001) Experimental evidence for testis size evolution via sperm competition. Ecology Letters, 4, 10–13. Hughes, W.H.O. and Boomsma, J.J. (2006) Does genetic diversity hinder parasite evolution in social insect colonies? Journal of Evolutionary Biology, 19, 132–143. Hughes, K. and Sokolowski, M.B. (1996) Natural selection in the laboratory for a change in resistance by Drosophila melanogaster to the parasitoid wasp Asobara tabida. Journal of Insect Behavior, 9, 477–491. Hume, J.C.C., Hamilton III, H., Lee, K.L. and Lehmann, T. (2011) Susceptibility of Anopheles stephensi to Plasmodium gallinaceum: a trait of the mosquito, the parasite, and the environment. PLoS ONE, 6: e20156. Ingleby, F.C., Lewis, Z. and Wedell, N. (2010) Level of sperm competition promotes evolution of male ejaculate allocation patterns in a moth. Animal Behaviour, 80, 37–43. Ironside, J.E. (2007) Multiple losses of sex within a single genus of microsporidia. BMC Evolutionary Biology, 7: 16.

 C 2013

Jaenike, J. (1978) An hypothesis to account for the maintenance of sex within populations. Evolutionary Theory, 1, 1–30. Katsuki, M., Harano, T., Miyatake, T., Okada, K. and Hosken, D.J. (2012) Intralocus sexual conflict and offspring sex ratio. Ecology Letters, 15, 193–197. Kawecki, T.J., Lenski, R.E., Ebert, D., Hollis, B., Olivieri, I. and Whitlock, M.C. (2012) Experimental evolution. Trends in Ecology and Evolution, 27, 547–560. Kerstes, N.A.G., B´er´enos, C. and Martin, O.Y. (2013) Coevolving parasites and population size shape the evolution of mating behaviour. BMC Evolutionary Biology, 13, 29. Kerstes, N.A.G., B´er´enos, C., Schmid-Hempel, P. and Wegner, K.M. (2012) Antagonistic experimental coevolution with a parasite increases host recombination frequency. BMC Evolutionary Biology, 12: 18. Kerstes, N.A.G. and Wegner, K.M. (2011) The effect of inbreeding and outcrossing of Tribolium castaneum on resistance to the parasite Nosema whitei. Evolutionary Ecology Research, 13, 681–696. Klingler, M. (2004) Tribolium–quick guide. Current Biology, 14, R639–R640. Knell, R.J., Begon, M. and Thompson, D.J. (1998) Transmission of Plodia interpunctella granulosis virus does not conform to the mass action model. Journal of Animal Ecology, 67, 592–599. Koch, H. and Schmid-Hempel, P. (2011) Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proceedings of the National Academy of Sciences of the United States of America, 108, 19288–19292. Koella, J.C. and Agnew, P. (1999) A correlated response of a parasite’s virulence and life cycle to selection on its host’s life history. Journal of Evolutionary Biology, 12, 70–79. Koella, J.C. and Bo¨ete, C. (2002) A genetic correlation between age at pupation and melanization immune response of the yellow fever mosquito Aedes aegypti. Evolution, 56, 1074– 1079. Koella, J.C. and Offenberg, J. (1999) Food availability and parasite infection influence the correlated responses of life history traits to selection for age at pupation in the mosquito Aedes aegypti. Journal of Evolutionary Biology, 12, 760–769. Kraaijeveld, A.R. and Godfray, H.C.J. (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature, 389, 278–280. Kraaijeveld, A.R. and Godfray, H.C.J. (2008) Selection for resistance to a fungal pathogen in Drosophila melanogaster. Heredity, 100, 400–406. Kraaijeveld, A.R., Layen, S.J., Futerman, P.H. and Godfray, H.C.J. (2012) Lack of phenotypic and evolutionary crossresistance against parasitoids and pathogens in Drosophila melanogaster. PLoS ONE, 7: e53002. Kraaijeveld, A.R., Limentani, E.C. and Godfray, H.C.J. (2001) Basis of the trade-off between parasitoid resistance and larval

Institute of Zoology, Chinese Academy of Sciences, 21, 401–414

Experimental host–parasite coevolution competitive ability in Drosophila melanogaster. Nature, 389, 278–280. Lawniczak, M.K., Barnes, A.I., Linklater, J.R., Boone, J.M., Wigby, S. and Chapman, T. (2007) Mating and immunity in invertebrates. Trends in Ecology and Evolution, 22, 48–55. Lazzaro, B.P. and Little, T.J. (2009) Immunity in a variable world. Philosophical Transactions of the Royal Society of London B (Biological Sciences), 364, 15–26. Lindfield, S. (1990) Microevolution in an insect–virus interaction. PhD thesis, University of Liverpool, UK. Ma, J., Benson, A.K., Kachman, S.D., Hu, Z. and Harshman, L.G. (2012) Drosophila melanogaster selection for survival of Bacillus cereus infection: life history trait indirect responses. International Journal of Evolutionary Biology, 2012, Article ID 935970. McNamara, K.B., Wedell, N. and Simmons, L.W. (2013) Experimental evolution reveals trade-offs between mating and immunity. Biology Letters, 9, 20130262. Maklakov, A.A., Bonduriansky, R. and Brooks, R.S. (2009) Sex differences, sexual selection and ageing: an experimental evolution approach. Evolution, 63, 2491–2503. Maklakov, A.A., Cayetano, L., Brooks, R.S. and Bonduriansky, R. (2010) The roles of life-history selection and sexual selection in the adaptive evolution of mating behaviour in a beetle. Evolution, 64, 1273–1282. Martin, O.Y. and Hosken, D.J. (2003a) The evolution of reproductive isolation through sexual conflict. Nature, 423, 979– 982. Martin, O.Y. and Hosken, D.J. (2003b) Costs and benefits of evolving under experimentally enforced polyandry or monogamy. Evolution, 57, 2765–2772. Martin, O.Y. and Hosken, D.J. (2004) Reproductive consequences of population divergence through sexual conflict. Current Biology, 14, 906–910. Martin, O.Y., Hosken, D.J. and Ward, P.I. (2004) Postcopulatory sexual selection decreases female fitness in Scathophaga stercoraria. Proceedings of the Royal Society of London B (Biological Sciences), 271, 353–359. Michalczyk, L., Millard, A.L., Martin, O.Y., Lumley, A., Emerson, B.C. and Gage, M.J.G. (2011a) Experimental evolution exposes female and male responses to sexual selection and conflict in Tribolium castaneum. Evolution, 65, 713– 724. Michalczyk, L., Millard, A.L., Martin, O.Y., Lumley, A., Emerson, B.C., Chapman, T. and Gage, M.J.G. (2011b) Inbreeding promotes female promiscuity. Science, 333, 1739– 1742. Miller, G.T. and Pitnick, S. (2002) Sperm-female coevolution in Drosophila. Science, 298, 1230–1233. Morrow, E.H. and Gage, M.J.G. (2001) Artificial selection and heritability of sperm length in Gryllus bimaculatus. Heredity, 87, 356–362.

 C 2013

413

Otti, O. (2007) Host-parasite interactions – experimental studies on virulence and transmission. PhD thesis, ETH Z¨urich. http://dx.doi.org/10.3929/ethz-a-005415249. Pijpe, J., Fischer, K., Brakefield, P.M. and Zwaan, B.J. (2006) Consequences of artificial selection on pre-adult development for adult lifespan under benign conditions in the butterfly Bicyclus anynana. Mechanisms of Ageing and Development, 127, 802–807. Rolff, J. and Kraaijeveld, A.R. (2003) Selection for parasitoid resistance alters mating success in Drosophila. Proceedings of the Royal Society of London B (Biological Sciences), 270, S154–S155. Rolff, J. and Siva-Jothy, M.T. (2002) Copulation corrupts immunity: a mechanism for a cost of mating in insects. Proceedings of the National Academy of Sciences of the United States of America, 99, 9916–9918. Sait, S.M., Begon, M. and Thompson, D.J. (1994) Long-term population dynamics of the Indian meal moth Plodia interpunctella and its granulosis virus. Journal of Animal Ecology, 63, 861–870. Salathe, M., Kouyos, R.D., Regoes, R.R. and Bonhoeffer, S. (2008) Rapid parasite adaptation drives selection for high recombination rates. Evolution, 62, 295–300. Sbilordo, S.H., Grazer, V.M., Demont, M. and Martin, O.Y. (2011) Impacts of starvation on male reproductive success in Tribolium castaneum. Evolutionary Ecology Research, 13, 347–359. Scharf, I., Peter, F. and Martin, O.Y. (2013) Reproductive tradeoffs and direct costs for males in arthropods. Evolutionary Biology, 40, 169–184. Schulte, R.D., Makus, C., Hasert, B., Michiels, N.K. and Schulenburg, H. (2010) Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proceedings of the National Academy of Sciences of the United States of America, 107, 7359–7364. Schwarzenbach, G.A. and Ward, P.I. (2006) Responses to selection on phenoloxidase activity in yellow dung flies. Evolution, 60, 1612–1621. Schwarzenbach, G.A. and Ward, P.I. (2007) Phenoloxidase activity and pathogen resistance in yellow dung flies Scathophaga stercoraria. Journal of Evolutionary Biology, 20, 2192–2199. Simmons, L.W. and Garcia-Gonzalez, F. (2008) Evolutionary reduction in testes size and comparative fertilization success in response to the experimental removal of sexual selection in dung beetles. Evolution, 62, 2580–2591. Siva-Jothy, M.T., Tsubaki, Y. and Hooper, R.E. (1998) Decreased immune response as a proximate cost of copulation and oviposition in a damselfly. Physiological Entomology, 23, 274–277. Sokoloff, A. (1974) The Biology of Tribolium. Oxford University Press, Oxford, UK.

Institute of Zoology, Chinese Academy of Sciences, 21, 401–414

414

N. A. G. Kerstes & O. Y. Martin

The Tribolium Genome Sequencing Consortium (2008) The genome of the model beetle and pest Tribolium castaneum. Nature, 452, 949–955. Thompson, R.C.A. and Lymbery, A.J. (1996) Genetic variability in parasites and host-parasite interactions. Parasitology, 112, S7–S22. Tigreros, N. and Lewis, S.M. (2011) Direct and correlated responses to artificial selection on sexual size dimorphism in the flour beetle, Tribolium castaneum. Journal of Evolutionary Biology, 24, 835–842. Trienens, M. and Rohlfs, M. (2011) Experimental evolution of defense against a competitive mold confers reduced sensitivity to fungal toxins but no increased resistance in Drosophila larvae. BMC Evolutionary Biology, 11, 206. van Baalen, M. and Sabelis, M.W. (1995) The dynamics of multiple infection and the evolution of virulence. American Naturalist, 146, 881–910. Webster, J.P. and Woolhouse, M.E.J. (1999) Cost of resistance: relationship between reduced fertility and increased resistance in a snail-schistosome host-parasite system. Proceedings of the Royal Society of London B (Biological Sciences), 266, 391–396. Wegner, K.M., B´er´enos, C. and Schmid-Hempel, P. (2008) Nonadditive genetic components in resistance of the red flour bee-

 C 2013

tle Tribolium castaneum against parasite infection. Evolution, 62, 2381–2392. Wegner, K.M., B´er´enos, C. and Schmid-Hempel, P. (2009) Host genetic architecture in single and multiple infections. Journal of Evolutionary Biology, 22, 396–404. Wigby, S. and Chapman, T. (2004) Female resistance to male harm evolves in response to manipulation of sexual conflict. Evolution, 58, 1028–1037. Wit, J., Sarup, P., Lupsa, N., Malte, H., Frydenberg, J. and Loeschke, V. (2013) Longevity for free? Increased reproduction with limited trade-offs in Drosophila melanogaster selected for increased life span. Experimental Gerontology, 48, 349–357. Ye, Y.E., Chenoweth, S.F. and McGraw, E.A. (2009) Effective but costly, evolved mechanisms of defense against a virulent opportunistic pathogen in Drosophila melanogaster. PLoS Pathogens, 5, e1000385. Zou, Z., Evans, J.D., Lu, Z.Q., Zhao, P.C., Williams, M., Sumathipala, N., Hetru, C., Hultmark, D. and Jiang, H.B. (2007) Comparative genomic analysis of the Tribolium immune system. Genome Biology, 8, R177.

Accepted September 29, 2013

Institute of Zoology, Chinese Academy of Sciences, 21, 401–414

Insect host-parasite coevolution in the light of experimental evolution.

The many ways parasites can impact their host species have been the focus of intense study using a range of approaches. A particularly promising but u...
176KB Sizes 0 Downloads 0 Views