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Evolution of guppies' resistance and tolerance to their Gyrodactylus parasites. (a) Difference in average G. turnbulli peak load (a measure of resistance) versus average difference in survival (day of death-a measure of tolerance), and (b) average cumulative parasite load from day 0 to 10 (resistance) versus change in relative condition index (K n ) between day 0 and 10 of infection (tolerance). All differences (Dparasite load, Dsurvival and DK n ) are relative differences between the Lower Lalaja (LL), Upper Lalaja (UL), Taylor (T) and Caigual (C) introductions, and the Guanapo source population (S), from the 2010 collection. Non-zero values suggest evolution in a given direction. Quadrants I and III indicate a negative correlation (trade-off) between resistance and tolerance. Error bars are +1 s.e.m. 

Evolution of guppies' resistance and tolerance to their Gyrodactylus parasites. (a) Difference in average G. turnbulli peak load (a measure of resistance) versus average difference in survival (day of death-a measure of tolerance), and (b) average cumulative parasite load from day 0 to 10 (resistance) versus change in relative condition index (K n ) between day 0 and 10 of infection (tolerance). All differences (Dparasite load, Dsurvival and DK n ) are relative differences between the Lower Lalaja (LL), Upper Lalaja (UL), Taylor (T) and Caigual (C) introductions, and the Guanapo source population (S), from the 2010 collection. Non-zero values suggest evolution in a given direction. Quadrants I and III indicate a negative correlation (trade-off) between resistance and tolerance. Error bars are +1 s.e.m. 

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A reduction in the strength of selection is expected to cause the evolution of reduced trait expression. Elimination of a parasite should thus cause the evolution of reduced resistance to that parasite. To test this prediction in nature, we studied the fourth- and eighth-generation descendants of guppies (Poecilia reticulata) introduced into four n...

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... all of the guppy populations, G. turnbulli infection showed a typical phase of rapid increase that decelerated until reaching a peak and finally crashed ( figure 2a,c,e). Start- ing at day 8 of infection, average parasite load began to differ Table 1. Guppy survival as a measure of tolerance. (Cox proportional hazards results for survival until end of experiment with 'day of death' as a response variable, and 'population of origin' and 'parasite peak load' as explanatory variables. Values are for individuals of a given introduction site relative to the source population. Higher tolerance is indicated by higher survival for a given parasite load at peak (i.e. significant interaction coefficient notably among the populations. We used three common and robust metrics to quantify this variation in guppy resistance to G. turnbulli: peak load, load on day 10 and the parasite intrinsic rate of increase (r). Relative to the source population, both peak load and load on day 10 were significantly lower (and resistance therefore higher) for (i) two of the four intro- duced populations (Upper Lalaja and Taylor) studied after 1 year of evolution in nature, and (ii) both introduced popu- lations (Upper Lalaja and Lower Lalaja) studied after 2 years of evolution in nature (table 2 and figure 2). In the first case, another of the introduced populations (Caigual) also showed evidence of increased resistance based on load on day 10. Relative to the source population, r was significantly lower (and resistance therefore higher) for (i) one of the four intro- duced populations (Taylor) after 1 year of evolution in nature (figure 2f and table 3), and (ii) both of the introduced popu- lations after 2 years of evolution in nature (figure 2d and table 3). In summary, none of the guppy populations relea- sed from parasite (Gyrodactylus) pressure evolved decreased resistance to that parasite: instead, most evidence pointed toward a rapid evolution of increased resistance. The evolution of increased resistance in the absence of a parasite might reflect a correlated response to the evolution of decreased tolerance (the host's ability to reduce the damage caused by a given number of parasites). We measured tolerance as a population's slope of survival in relation to peak parasite load (higher survival for a given parasite load would mean increased tolerance) and as change in relative condition index in relation to cumulative parasite load in the first 10 days of infection (higher condition for a given parasite load would mean increased tolerance). Using these metrics, no evidence was found of the evolution of decreased tolerance: relative to guppies from the source population, guppies from the introduced populations did not have lower survival rates for a given parasite load (table 1) or lower condition (see the electronic supplementary material, appendix S3). If anything, the trend was toward increased tolerance in the introduced populations ( figure 3a). Furthermore, we found no evidence of a negative association between measures of resistance and measures of tolerance (figure 3a,b)-as would have been expected if the evolution of decreased tolerance caused a correlated response toward increased ...

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... As ectoparasites, Gyrodactylus can directly be observed and counted, instead of relying on invasive methods preventing multiple observations of the same host, or alternatively, using indirect proxies of parasite load to obtain repeated observations. Therefore, several studies have used the Gyrodactylus-guppy system to investigate host-parasite interactions [21][22][23][24]. Yet, whether size-selective harvesting affects immune response to Gyrodactylus remains unstudied. ...
... This was done individually by bringing heavily infected donor fish that has been given an overdose of MS-222 into physical contact with the experimental fish, confirming the establishment of three parasites under a microscope, and facilitating the transfer with Dumont tweezers No.5 when needed. This method is similar to the ones used before [18,21,23,39,40]. ...
Article
Harvesting is typically size-selective, targeting large individuals. This is expected to lead to reduced average body size and earlier maturation (i.e. faster life histories). Such changes can also affect traits seemingly unrelated to harvesting, including immunocompetence. Here we test four hypotheses on how harvesting affects immunocompetence based on the pace-of-life syndrome, habitat area limitation and energy allocation and acquisition, respectively. We empirically evaluate these hypotheses using an experimental system consisting of the ectoparasite Gyrodactylus turnbulli and lines of guppies Poecilia reticulata that had been subjected to either small, random or large size-selective harvest for over 12 years. We followed the infection progression of individually infected fish for 15 days. We found significant differences between the harvested lines: fish from the small-harvested lines had the highest parasite loads. During the early phase of the infection, parasite loads were the lowest in the large-harvested lines, whereas the terminal loads were the lowest for the random-harvested lines. These results agree with the predictions from the energetic trade-off and surface area hypotheses. To our knowledge, this is the first demonstration of the consequences of size-selective harvesting on immunocompetence.
... Monogenean ectoparasites in the genus Gyrodactylus are widespread across wild guppy populations, but their prevalence varies greatly between and within populations, and through time (Dargent et al., 2013;Mohammed et al., 2020;van Oosterhout et al., 2003;Stephenson et al., 2015Stephenson et al., , 2017. The known pathogenicity of the parasites, coupled with the relative ease with which they can be maintained in a laboratory and used in exposure-controlled infection trials, make the guppy-Gyrodactylus system an excellent model for studying a wide range of host-parasite interactions, including the effects of parasitism on some of the processes described above (e.g., sexual selection, predator-prey; reviewed by Bakke et al., 2007). ...
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Natural host populations differ in their susceptibility to infection by parasites, and these intra‐population differences are still an incompletely understood component of host‐parasite dynamics. In this study, we used controlled infection experiments with wild‐caught guppies (Poecilia reticulata) and their ectoparasite Gyrodactylus turnbulli to investigate the roles of local adaptation and host genetic composition (immunogenetic and neutral) in explaining differences in susceptibility to infection. We found differences between our four study host populations that were consistent between two parasite source populations, with no indication of local adaptation by either host or parasite at two tested spatial scales. Greater host population genetic variability metrics broadly aligned with lower population mean infection intensity, with the best alignments associated with Major Histocompatibility Complex (MHC) ‘supertypes’. Controlling for intra‐population differences and potential inbreeding variance, we found a significant negative relationship between individual‐level functional MHC variability and infection: fish carrying more MHC supertypes experienced infections of lower severity, with limited evidence for supertype‐specific effects. We conclude that population‐level differences in host infection susceptibility likely reflect variation in parasite selective pressure and/or host evolutionary potential, underpinned by functional immunogenetic variation.
... The research of guppies in Trinidad has primarily focused on the interplay of predation and sexual selection, while studies on parasite-mediated selection are relatively underrepresented. As with predation, parasite-mediated selection pressures can drive parallel evolution in guppy coloration, behaviour and life history among populations [7][8][9]. Colour expression may be negatively correlated with parasite infection [10,11], i.e. parasitized male guppies devote less energy to mating and courtship and display less intense mating colours, thereby appearing less fit and attractive to females [10,12]. ...
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The guppy (Poecilia reticulata) is a model species in ecology and evolution. Many studies have examined effects of predators on guppy behaviour, reproduction, survival strategies, feeding and other life-history traits, but few have studied variation in their parasite diversity. We surveyed parasites of 18 Trinidadian populations of guppy, to provide insight on the geographical mosaic of parasite variability, which may act as a source of natural selection acting on guppies. We found 21 parasite species, including five new records for Trinidad. Spatial variation in parasite diversity was significantly higher than that of piscine predators, and significant variation in parasite richness among individuals and populations was correlated with: (i) host size, (ii) snail species richness, and (iii) the distance between populations. Differences in parasite species richness are likely to play an important, yet underestimated role in the biology of this model species of vertebrate ecology and evolution.
... Another limitation is our assumption of homogeneity of hosts, which is not accurate in this system. Guppies are known to exhibit a broad range in both life history traits (Reznick and Endler, 1982;Gordon et al., 2009) and innate resistance to parasites (Fraser et al., 2009;Fraser and Neff, 2010;Dargent et al., 2013), both within and among populations. Additionally, individual guppies may vary in their susceptibility to parasites due to individual characteristics such as size (Cable and van Oosterhout, 2007;Tadiri et al., 2013), carotenoid coloration (Grether et al., 2004;Kolluru et al., 2006) and sex (Richards et al., 2010(Richards et al., , 2012Dargent et al., 2016;Tadiri et al., 2016). ...
... Our parameters don't capture the wide variability that occurs in nature, or how this heterogeneity may influence host-parasite dynamics in the population but were instead based on average values obtained from literature and our own laboratory observations. Moreover, significant variability even in average population-level resistance has been observed among wild populations and domestic fish to various strains of gyrodactylids (Van Oosterhout et al., 2003;Cable and van Oosterhout, 2007;Dargent et al., 2013, Pérez-Jvostov et al., 2015 and it's possible that our estimated parameters may not fit some extreme cases of particularly low-or high-resistance population. However, despite not accounting for such complexities, our model fit data from two experiments, one which used fish from various wild populations from Trinidad and one which used domestic fish, therefore we find these average values to be a decent approximation. ...
Article
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The use of model experimental systems and mathematical models is important to further understanding of infectious disease dynamics and strategize disease mitigation. Gyrodactylids are helminth ectoparasites of teleost fish which have many dynamical characteristics of microparasites but offer the advantage that they can be quantified and tracked over time, allowing further insight into within-host and epidemic dynamics. In this paper, we design a model to describe host-parasite dynamics of the well-studied guppy-Gyrodactylus turnbulli system, using experimental data to estimate parameters and validate it. We estimate the basic reproduction number (R0), for this system. Sensitivity analysis reveals that parasite growth rate, and the rate at which the guppy mounts an immune response have the greatest impact on outbreak peak and timing both for initial outbreaks and on longer time scales. These findings highlight guppy population average resistance and parasite growth rate as key factors in disease control, and future work should focus on incorporating heterogeneity in host resistance into disease models and extrapolating to other host-parasite systems.
... Another limitation is our assumption of homogeneity of hosts, which is not accurate in this system. Guppies are known to exhibit a broad range in both life history traits (Reznick and Endler, 1982;Gordon et al., 2009) and innate resistance to parasites (Fraser et al., 2009;Fraser and Neff, 2010;Dargent et al., 2013), both within and among populations. Additionally, individual guppies may vary in their susceptibility to parasites due to individual characteristics such as size (Cable and van Oosterhout, 2007;Tadiri et al., 2013), carotenoid coloration (Grether et al., 2004;Kolluru et al., 2006) and sex (Richards et al., 2010(Richards et al., , 2012Dargent et al., 2016;Tadiri et al., 2016). ...
... Our parameters don't capture the wide variability that occurs in nature, or how this heterogeneity may influence host-parasite dynamics in the population but were instead based on average values obtained from literature and our own laboratory observations. Moreover, significant variability even in average population-level resistance has been observed among wild populations and domestic fish to various strains of gyrodactylids (Van Oosterhout et al., 2003;Cable and van Oosterhout, 2007;Dargent et al., 2013, Pérez-Jvostov et al., 2015 and it's possible that our estimated parameters may not fit some extreme cases of particularly low-or high-resistance population. However, despite not accounting for such complexities, our model fit data from two experiments, one which used fish from various wild populations from Trinidad and one which used domestic fish, therefore we find these average values to be a decent approximation. ...
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The use of model experimental systems and mathematical models is important to further understanding of infectious disease dynamics and strategize disease mitigation. Gyrodactylids are helminth ectoparasites of teleost fish which have many dynamical characteristics of microparasites but offer the advantage that they can be quantified and tracked over time, allowing further insight into within-host and epidemic dynamics. In this paper, we design a model to describe host-parasite dynamics of the well-studied guppy-Gyrodactylus turnbulli system, using experimental data to estimate parameters and validate it. We estimate the basic reproduction number (R_0), for this system. Sensitivity analysis reveals that parasite growth rate, and the rate at which the guppy mounts an immune response have the greatest impact on outbreak peak and timing both for initial outbreaks and on longer time scales. These findings highlight guppy population resistance and parasite virulence as key factors in disease control, and future work should focus on incorporating heterogeneity in host resistance into disease models and extrapolating to other host-parasite systems.
... Adaptation to those other environmental changes was presumably more important than the resulting correlated maladaptation to changes in parasites. Dargent et al. 2013Dargent et al. , 2016 Roadside frogs Wood frogs exposed to high-salt environments beside roads perform poorly in all environments, whether salty or not. ...
Article
Evolutionary biologists have long trained their sights on adaptation, focusing on the power of natural selection to produce relative fitness advantages while often ignoring changes in absolute fitness. Ecologists generally have taken a different tack, focusing on changes in abundance and ranges that reflect absolute fitness while often ignoring relative fitness. Uniting these perspectives, we articulate various causes of relative and absolute maladaptation and review numerous examples of their occurrence. This review indicates that maladaptation is reasonably common from both perspectives, yet often in contrasting ways. That is, maladaptation can appear strong from a relative fitness perspective, yet populations can be growing in abundance. Conversely, resident individuals can appear locally adapted (relative to nonresident individuals) yet be declining in abundance. Understanding and interpreting these disconnects between relative and absolute maladaptation, as well as the cases of agreement, is increasingly critical in the face of accelerating human-mediated environmental change. We therefore present a framework for studying maladaptation, focusing in particular on the relationship between absolute and relative fitness, thereby drawing together evolutionary and ecological perspectives. The unification of these ecological and evolutionary perspectives has the potential to bring together previously disjunct research areas while addressing key conceptual issues and specific practical problems.
... Infection with the common (Harris and Lyles 1992) monogenean ectoparasite Gyrodactylus spp. has detrimental consequences for guppy fitness (van Oosterhout et al. 2007;Pérez-Jvostov et al. 2012;Dargent et al. 2013), and influences MHC evolution (Fraser and Neff 2009;Fraser et al. 2010), association preferences, mate choice, and male signaling traits (Kennedy et al. 1987;Houde and Torio 1992;Lopez 1998;Kolluru et al. 2009). Individuals moving from low-predation to high-predation environments are strongly selected against and traits under divergent selection from predators also influence mate choice (Endler and Houde 1995). ...
... At the introduction sites, by contrast, Gyrodactylus spp. are absent (Dargent et al. 2014), large piscivorous predators are absent, productivity is lower, and invertebrate availability is lower (Zandonà et al. 2011;Kohler et al. 2012;Dargent et al. 2013;Arendt et al. 2014). Furthermore, other unmeasured factors differ between the introduction sites and the source population, such as stream morphology, as well as population age and fish size distributions, which influence intraspecific competition, and ultimately influence trait divergence and local adaptation (Torres Dowdall et al. 2012). ...
... In 2011, guppies were collected from the source and introduction sites, transported to laboratory facilities, and raised for 2 generations in a common-garden environment (for details, see Dargent et al. 2013). For this reason, any observed difference among the populations in suites of traits, including female mate preference, likely reflects genetic effects rather than plasticity or maternal effects, while also limiting the potential effects of selection under laboratory conditions for more generations (Reznick et al. 1990). ...
Article
Progress toward local adaptation is expected to be enhanced when divergent selection is multidimensional, because many simultaneous sources of selection can increase the total strength of selection and enhance the number of independent traits under selection. Yet, whether local adaptation ensues from multidimensional selection also depends on its potential to cause the build-up of reproductive barriers such as sexual signals and preference for these signals. We used replicate experimental introductions of guppies (Poecilia reticulata) in nature to test whether an abrupt and dramatic shift in multiple important ecological dimensions (at a minimum: parasitism, predation, and diet/resources) promoted the contemporary evolution of assortative mating. After 8–12 postintroduction guppy generations in the wild, we bred descendants of each population in a common-garden laboratory environment for 2 generations, after which we recorded the preferences of females from each population for males from all populations. We found contemporary evolution of male traits (size, body condition, color) that should influence mate choice, but no evidence for the occurrence of positive assortative preferences. That is, females in a given evolving population did not prefer males from that population over males from other populations. Instead, females tended to prefer novel males (i.e., disassortative mating), which likely acts as a mechanism preventing the evolution of reproductive isolation. Preferences for novelty may explain why many cases of local adaptation do not lead to the evolution of reproductive barriers and ecological speciation.
... One of the key processes is the coevolution between hosts and parasites. Parasites shape the immune function of their host and in response undergo rapid evolution of virulence, which may result in ongoing antagonistic coevolution (Buckling & Rainey, 2002;Dargent, Scott, Hendry, & Fussmann, 2013;Eizaguirre, Lenz, Kalbe, & Milinski, 2012;Paterson et al., 2010). However, the underlying evolutionary trajectories of this coevolution have mostly been studied in species pairs. ...
Article
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Parasites are one of the strongest selective agents in nature. They select for hosts that evolve counter‐adaptive strategies to cope with infection. Helminth parasites are special because they can modulate their hosts’ immune responses. This phenomenon is important in epidemiological contexts, where co‐infections may be affected. How different types of hosts and helminths interact with each other is insufficiently investigated. We used the three‐spined stickleback (Gasterosteus aculeatus) – Schistocephalus solidus model to study mechanisms and temporal components of helminth immune modulation. Sticklebacks from two contrasting populations with either high resistance (HR) or low resistance (LR) against S. solidus, were individually exposed to S. solidus strains with characteristically high growth (HG) or low growth (LG) in G. aculeatus. We determined the susceptibility to another parasite, the eye fluke Diplostomum pseudospathaceum, and the expression of 23 key immune genes at three time points after S. solidus infection. D. pseudospathaceum infection rates and the gene expression responses depended on host and S. solidus type and changed over time. Whereas the effect of S. solidus type was not significant after three weeks, T regulatory responses and complement components were up‐regulated at later time points if hosts were infected with HG S. solidus. HR hosts showed a well‐orchestrated immune response, which was absent in LR hosts. Our results emphasize the role of regulatory T cells and the timing of specific immune responses during helminth infections. This study elucidates the importance to consider different co‐evolutionary trajectories and ecologies when studying host‐parasite interactions. This article is protected by copyright. All rights reserved.
... In particular, the tropical Trinidadian guppy-Gyrodactylus turnbulli system has been utilised extensively to investigate social behaviour (e.g. Edenbrow et al., 2011), evolutionary ecology (Pérez-Jvostov et al., 2012;Dargent et al., 2013), and epidemiology (Stephenson et al., 2015;Smallbone et al., 2016). The parasite's direct life cycle, short generation time (ca. ...
Article
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Many freshwater habitats are subject to change through time. Specifically, natural flow regimes are substantially modified by not only seasonal climatic change, but also anthropogenic activity. Consequently, freshwater organisms are exposed to variable flow, potentially altering their behaviour and subsequently parasite transmission amongst social hosts. Here, we investigate the effects of flow conditions on the shoaling behaviour of Trinidadian guppies (Poecilia reticulata), and the resulting transmission of a directly transmitted ectoparasite, Gyrodactylus turnbulli. Shoals exposed to continuous flow exhibited significantly greater G. turnbulli peak intensities and abundance when compared to fish subjected to interrupted, but not no-flow conditions. Parasite transmission rate was greater in shoals exposed to interrupted flow, resulting in parasites becoming more distributed amongst shoal members and thus reducing mean intensity in comparison to continuous flow shoals. Furthermore, as prevalence increased, the distance between shoaling conspecifics increased at greater rates in interrupted and no-flow conditions compared to continuous flow: indicating that in the absence of flowing water, parasitism has a greater effect on shoaling decisions. This data highlights how fish behaviourally respond to variable flow conditions and the implications for parasite transmission.
... The Trinidadian guppy (Poecilia reticulata; Figure 1) is considered emblematic of parallel and convergent evolution, wherein many adaptive traits have repeatedly and predictably evolved in response to strong natural selection (Endler, 1995;Magurran, 2005;Oke et al., 2017). For instance, populations experiencing different predation regimes (high-predation vs. low-predation) exhibit different color patterns (Endler, 1978), color amounts (Gotanda & Hendry, 2014;Winemiller, Leslie, & Roche, 1990), life histories (Reznick & Endler, 1982;Reznick, Rodd, & Cardenas, 1996), opsin genes (Sandkam, Young, & Breden, 2015), morphologies (Hendry, Kelly, Kinnison, & Reznick, 2006), parasite resistance (Dargent, Scott, Hendry, & Fussmann, 2013), and behaviors (Burns, Price, Thomson, Hughes, & Rodd, 2016;Houde & Endler, 1990;Kelley & Magurran, 2003;O'Steen, Cullum, & Bennett, 2002). However, various studies have also identified nonparallel aspects to this divergence, including for color (Kemp, Reznick, Grether, & Endler, 2009;Millar & Hendry, 2012), female preferences (Endler & Houde, 1995;Houde & Endler, 1990), life history (Fitzpatrick, Torres-Dowdall, Reznick, Ghalambor, & Funk, 2014), morphologies (Odell, Chappell, & Dickson, 2003), parasite resistance (Pérez-Jvostov, Hendry, Fussmann, & Scott, 2015), and behavior (Jacquin et al., 2016). ...
Article
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The Trinidadian guppy is emblematic of parallel and convergent evolution, with repeated demonstrations that predation regime is a driver of adaptive trait evolution. A classic and foundational experiment in this system was conducted by John Endler 40 years ago, where male guppies placed into low‐predation environments in the laboratory evolved increased color in a few generations. However, Endler's experiment did not employ the now typical design for a parallel/convergent evolution study, which would employ replicates of different ancestral lineages. We therefore implemented an experiment that seeded replicate mesocosms with small founding populations of guppies originating from high‐predation populations of two very different lineages. The different mesocosms were maintained identically, and male guppy color was quantified every four months. After one year, we tested whether male color had increased, whether replicates within a lineage had parallel phenotypic trajectories, and whether the different lineages converged on a common phenotype. Results showed that male guppy color generally increased through time, primarily due to changes in melanic color, whereas the other colors showed inconsistent and highly variable trajectories. Most of the nonparallelism in phenotypic trajectories was among mesocosms containing different lineages. In addition to this mixture of parallelism and nonparallelism, convergence was not evident in that the variance in color among the mesocosms actually increased through time. We suggest that our results reflect the potential importance of high variation in female preference and stochastic processes such as drift and founder effects, both of which could be important in nature.