Parting ways: parasite release in nature leads to sex‐specific evolution of defence

We evaluated the extent to which males and females evolve along similar or different trajectories in response to the same environmental shift. Specifically, we used replicate experimental introductions in nature to consider how release from a key parasite (Gyrodactylus) generates similar or different defence evolution in male vs. female guppies (Poecilia reticulata). After 4–8 generations of evolution, guppies were collected from the ancestral (parasite still present) and derived (parasite now absent) populations and bred for two generations in the laboratory to control for nongenetic effects. These F2 guppies were then individually infected with Gyrodactylus, and infection dynamics were monitored on each fish. We found that parasite release in nature led to sex‐specific evolutionary responses: males did not show much evolution of resistance, whereas females showed the evolution of increased resistance. Given that male guppies in the ancestral population had greater resistance to Gyrodactylus than did females, evolution in the derived populations led to reduction of sexual dimorphism in resistance. We argue that previous selection for high resistance in males constrained (relative to females) further evolution of the trait. We advocate more experiments considering sex‐specific evolutionary responses to environmental change.     

Pace of life,predators and parasites: predator-induced life-history evolution in Trinidadian guppies predicts decrease in parasite tolerance

A common evolutionary response to predation pressure is increased investment in reproduction, ultimately resulting in a fast life history. Theory and comparative studies suggest that short-lived organisms invest less in defence against parasites than those that are longer lived (the pace of life hypothesis). Combining these tenets of evolutionary theory leads to the specific, untested prediction that within species, populations experiencing higher predation pressure invest less in defence against parasites. The Trinidadian guppy, Poecilia reticulata, presents an excellent opportunity to test this prediction: guppy populations in lower courses of rivers experience higher predation pressure, and as a consequence have evolved faster life histories, than those in upper courses. Data from a large-scale field survey showed that fish infected with Gyrodactylus parasites were of a lower body condition (quantified using the scaled mass index) than uninfected fish, but only in lower course populations. Although the evidence we present is correlational, it suggests that upper course guppies sustain lower fitness costs of infection, i.e. are more tolerant, than lower course guppies. The data are therefore consistent with the pace of life hypothesis of parasite defence allocation, and suggest that life-history traits mediate the indirect effect of predators on the parasites of their prey.     

Interactions Between Competition and Predation Shape Early Growth and Survival of Two Neotropical Hylid Tadpoles

Experimental studies in temperate regions have revealed that competition and predation interact to shape aquatic communities. Predators typically reduce the effect of competition on growth and competitors provide alternative prey subjects, which may also alter predation. Here, we examine the independent and combined effects of competition and predation on the survival and growth of hatchling tadpoles of two widespread co‐occurring Neotropical hylid frogs (Agalychnis callidryas and Dendropsophus ebraccatus). Using 400 L mesocosms, we used a 2 × 3 factorial substitutive design, which crossed tadpole species composition with the presence or absence of a free‐roaming predator (Anax amazili dragonfly larva). Dragonflies were effective predators of both species, but had larger effects on A. callidryas survival. Both species had similar growth rates when alone, whereas A. callidryas grew 30 percent faster than D. ebraccatus when they co‐occurred, suggesting interspecific rather than intraspecific competition had relatively stronger effects on D. ebraccatus growth, while the opposite was true for A. callidryas. Predator presence dramatically reduced growth rates of both species and erased this asymmetry. Results suggest that the effects of predator induction (i.e., nonconsumptive effects) on growth were larger than both consumptive and competitive effects. Our study demonstrates that predators have strong effects on both survival and growth of prey, highlighting the potential importance of predators in shaping prey populations and tropical aquatic food web interactions. Abstract in Spanish is available at http://www.blackwell‐synergy.com/loi/btp .     

Local adaptation of fish consumers alters primary production through changes in algal community composition and diversity

Ecological research has focused on understanding how changes in consumer abundance affects community structure and ecosystem processes. However, there is increasing evidence that evolutionary changes in consumers can also alter community structure and ecosystem processes. Typically, the effects of consumer phenotype on communities and ecosystem processes are measured as net effects that integrate numerous ecological pathways. Here, we analyze new data from experimental manipulations of Trinidadian guppy Poecilia reticulata presence, density and phenotype to examine how effects on the algal community cause changes in gross‐primary production (GPP). We combine analytical tools borrowed from path analysis with experimental exclosures in mesocosms to separate the ecological and evolutionary effects of guppies into direct and indirect components. We show that the evolutionary effects of guppy phenotype act through different ecological pathways than the effects of guppy presence and density on GPP. As reported in previous studies that used a different measure of algal biomass, adding guppies and doubling their densities decreased algal biovolume through direct effects. In contrast to these previously reported results, exchanging guppy phenotypes that live without predators for phenotypes that live with predators did not affect algal biovolume. Instead, guppies from populations that live with predators increased the diversity of algal species and increased GPP compared to guppies that live without predators. These changes in the algal community were driven primarily by guppy phenotypes that live with predators—algal communities in mesocosms without fish were similar to those with guppies from predator‐free locations, but both were different from mesocosms with guppies from populations that live with predators. Changes in the algal community were driven directly by differences in foraging behavior between the two consumer phenotypes. We reconcile these results with our previous findings, thereby enhancing our understanding of the relationship between ecological and evolutionary processes.     

Competition and host size mediate larval anuran interactions with trematode parasites

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How might Gyrodactylus parasitism modify trade-offs between female preference and susceptibility of males to predation in Trinidadian guppies?

A number of examples exist of trade-offs between mating success and survival; that is, success in one fitness component comes at the cost of success in the other fitness component. However, these expected trade-offs are – perhaps even more commonly – not observed. One explanation for this apparent paradox of missing trade-offs could be that the other factors generating fitness variation across individuals confound or obscure the expected trade-off. These confounding effects could arise in two general ways: (i) the additional source of variation could positively (or negatively) influence both fitness components (“shared confounder” hypothesis), or (ii) the additional source of variation could influence only one fitness component (“non-shared confounder” hypothesis). We tested whether parasitism by Gyrodactylus spp. could be a confounder of trade-offs between female preference and susceptibility to predation for male Trinidadian guppies (Poecilia reticulata). As in previous work, we did not find the expected trade-off; that is, the males preferred by females were not more likely to be eaten by predators. Because half of the experimental males were infected by Gyrodactylus in a paired design, we were able to show that females discriminated against infected males, but that infected males were not more susceptible to predation. Our results thus provide support for the non-shared confounder hypothesis. That is, by negatively affecting one fitness component (female choice) but not the other (susceptibility to predation), parasitism by Gyrodactylus could obscure the expected trade-off between female preference and susceptibility to predation.     

Presence of soldier larvae determines the outcome of competition in a polyembryonic wasp

Soldier‐producing polyembryonic waSPS are the only social animals that develop as parasites inside the bodies of other insects. Characterizing the kin composition of broods is central to understanding the evolution of the soldier caste in these unique social insects. Here we studied the role of soldiers in mediating the outcome of competition among clones of the polyembryonic wasp Copidosoma floridanum. Soldier‐producing female clones usually monopolized host resources, whereas soldierless male clones usually coexisted in hosts. Behavioural experiments further indicated that early‐emerging soldiers are specialized to combat intraspecific competitors and later‐emerging soldiers are specialized for defence against interspecific competitors. Taken together, our results point to intraspecific competition as a major selective force in the evolution of the soldier caste. Our data also present an evolutionary conundrum: given the benefit of soldiers, why are male clones functionally soldierless?     

The association of feeding behaviour with the resistance and tolerance to parasites in recently diverged sticklebacks

Divergent natural selection regimes can contribute to adaptive population divergence, but can be sensitive to human‐mediated environmental change. Nutrient loading of aquatic ecosystems, for example, might modify selection pressures by altering the abundance and distribution of resources and the prevalence and infectivity of parasites. Here, we used a mesocosm experiment to test for interactive effects of nutrient loading and parasitism on host condition and feeding ecology. Specifically, we investigated whether the common fish parasite Gyrodactylus sp. differentially affected recently diverged lake and stream ecotypes of three‐spined stickleback (Gasterosteus aculeatus). We found that the stream ecotype had a higher resistance to Gyrodactylus sp. infections than the lake ecotype, and that both ecotypes experienced a cost of parasitism, indicated by negative relationships between parasite load and both stomach fullness and body condition. Overall, our results suggest that in the early stages of adaptive population divergence of hosts, parasites can affect host resistance, body condition and diet.     

Effects of nitrate on the interactions of the tadpoles of two ranids (Rana clamitans and R. catesbeiana)

Nitrogen pollution as a result of agricultural runoff and atmospheric deposition is a major challenge to aquatic ecosystems, and is likely to increase in the future. Nitrogenous pollutants are potential stressors of amphibian larvae through their toxicological impacts on individuals; however, they may also increase primary productivity. We examined how such an anthropogenic stressor could influence the interactions between two potentially competing species of tadpoles (Rana clamitans and R. catesbeiana). In a 42 d mesocosm experiment, R. catesbeiana survival, but not final mass, was reduced by nitrate addition. Rana catesbeiana survival was lower when in competition with R. clamitans than when only experiencing intraspecific competition. For R. clamitans, survival was not affected by nitrate addition or competition type. Rana clamitans in nitrate addition mesocosms were heavier than tadpoles from no nitrate mesocosms, and were heavier in intraspecific than in interspecific mesocosms. Our results suggest that nitrate can influence the performance of amphibian larvae, and that its effects could have complex effects on aquatic ecosystems.     

Implications of guppy (Poecilia reticulata) life‐history phenotype for mosquito control

Guppies (Poecilia reticulata) are frequently introduced to both natural and artificial water bodies as a mosquito control. Laboratory studies have demonstrated that guppies can consume large numbers of larval mosquitoes. Our study investigates how intraspecific variability in guppy phenotype affects their importance as a mosquito biocontrol and how habitat conditions (natural ponds vs. water storage containers) may influence insect biomass and guppy feeding. Using a blocked experimental design, we established stream‐side mesocosm ponds with half receiving gravel substrate to simulate pond‐bottom habitat. To provide realistic diet choices and insect abundances, we allowed the mesocosms to colonize naturally with aquatic insect larvae for 1 month before introducing guppies. We tested two distinct guppy phenotypes (from high‐ and low‐predation streams) alongside fish‐free controls. After 1 month, we measured insect biomass in the mesocosms and examined guppy gut contents to document direct predation. While overall insect biomass was not significantly different across the three fish treatments, we observed a significant reduction in mosquito biomass in fish treatments compared to fish‐free controls, as well as intraspecific differences in feeding. Overall insect biomass was significantly higher in mesocosms without gravel, while habitat condition had no effect on mosquito biomass. As guppy phenotype responds to changes in their environments, it is an important consideration for biocontrol policy to anticipate potential ecosystem effects. We close by relating our findings to other studies and by discussing the implications and potential risks of using guppies to control mosquitoes.     

The effects of competition on fitness depend on the sex of both competitors

In intraspecific competition, the sex of competing individuals is likely to be important in determining the outcome of competitive interactions and the way exposure to conspecifics during development influences adult fitness traits. Previous studies have explored differences between males and females in their response to intraspecific competition. However, few have tested how the sex of the competitors, or any interactions between focal and competitor sex, influences the nature and intensity of competition. We set up larval seed beetles Callosobruchus maculatus to develop either alone or in the presence of a male or female competitor and measured a suite of traits: development time, emergence weight; male ejaculate mass, copulation duration, and lifespan; and female lifetime fecundity, offspring egg–adult survival, and lifespan. We found effects of competition and competitor sex on the development time and emergence weight of both males and females, and also of an interaction between focal and competitor sex: Females emerged lighter when competing with another female, while males did not. There was little effect of larval competition on male and female adult fitness traits, with the exception of the effect of a female competitor on a focal female's offspring survival rate. Our results highlight the importance of directly measuring the effects of competition on fitness traits, rather than distant proxies for fitness, and suggest that competition with the sex with the greater resource requirements (here females) might play a role in driving trait evolution. We also found that male–male competition during development resulted in shorter copulation times than male–female competition, a result that remained when controlling for the weight of competitors. Although it is difficult to definitively tease apart the effects of social environment and access to resources, this result suggests that something about the sex of competitors other than their size is driving this pattern.     

VIRULENCE AND COMPETITIVENESS: TESTING THE RELATIONSHIP DURING INTER‐ AND INTRASPECIFIC MIXED INFECTIONS

Understanding the reasons why different parasites cause different degrees of harm to their hosts is an important objective in evolutionary biology. One group of models predicts that if hosts are infected with more than one strain or species of parasite, then competition between the parasites will select for higher virulence. While this idea makes intuitive sense, empirical data to support it are rare and equivocal. We investigated the relationship between fitness and virulence during both inter‐ and intraspecific competition for a fungal parasite of insects, Metarhizium anisopliae. Contrary to theoretical expectations, competition favored parasite strains with either a lower or a higher virulence depending on the competitor: when in interspecific competition with an entomopathogenic nematode, Steinernema feltiae, less virulent strains of the fungus were more successful, but when competing against conspecific fungi, more virulent strains were better competitors. We suggest that the nature of competition (direct via toxin production when competing against the nematode, indirect via exploitation of the host when competing against conspecific fungal strains) determines the relationship between virulence and competitive ability.     

Parallel and nonparallel behavioural evolution in response to parasitism and predation in Trinidadian guppies

Natural enemies such as predators and parasites are known to shape intraspecific variability of behaviour and personality in natural populations, yet several key questions remain: (i) What is the relative importance of predation vs. parasitism in shaping intraspecific variation of behaviour across generations? (ii) What are the contributions of genetic and plastic effects to this behavioural divergence? (iii) And to what extent are responses to predation and parasitism repeatable across independent evolutionary lineages? We addressed these questions using Trinidadian guppies (Poecilia reticulata) (i) varying in their exposure to dangerous fish predators and Gyrodactylus ectoparasites for (ii) both wild‐caught F0 and laboratory‐reared F2 individuals and coming from (iii) multiple independent evolutionary lineages (i.e. independent drainages). Several key findings emerged. First, a population's history of predation and parasitism influenced behavioural profiles, but to different extent depending on the behaviour considered (activity, shoaling or boldness). Second, we had evidence for some genetic effects of predation regime on behaviour, with differences in activity of F2 laboratory‐reared individuals, but not for parasitism, which had only plastic effects on the boldness of wild‐caught F0 individuals. Third, the two lineages showed a mixture of parallel and nonparallel responses to predation/parasitism, with parallel responses being stronger for predation than for parasitism and for activity and boldness than for shoaling. These findings suggest that different sets of behaviours provide different pay‐offs in alternative predation/parasitism environments and that parasitism has more transient effects in shaping intraspecific variation of behaviour than does predation.     

Multivariate analyses of morphometrical features from Gyrodactylus spp. (Monogenea) parasitising British salmonids: Light microscope based studies

Species determination within the genus Gyrodactylus Nordmann, 1832 is based upon subtle differences in marginal hook morphology and has long posed taxonomic problems. This study uses univariate and multivariate analyses in an attempt to elucidate the Gyrodactylus species parasitising British salmonids. A total of 389 parasites were collected at 69 of 227 localities sampled throughout the British Isles from four salmonid host species, Salmo salar, Salmo trutta, Oncorhynchus mykiss and a limited number of Salvelinus alpinus. A small number of known species of Gyrodactylus from outside the UK were also added to the data set. Morphometric data on the sclerites were collected from slide preparations of Gyrodactylus using light microscopy. Univariate statistics were used to select 11 of the 18 useful morphometric features defined by Malmberg (1970) on the basis of those with the smallest natural variability and/or measurement error. The data, relating to the 11 variables chosen, were then analysed using principal components analysis (PCA) to describe the forms present. Initial outliers included foreign species of Gyrodactylus and an accidental infection by a gasterosteid form. Two major groups were resolved: one on S. salar and O. mykiss, the specimens from which resembled G. derjavini Mikailov, 1975 and G. caledoniensis Shinn et al. in press; and one on S. trutta, which was identified as G. truttae Gläser, 1974. The analysis, in addition to showing which were useful morphometric features, also demonstrated the limitations of data obtained from the smallest features when using the light microscope.     

INFLUENCE OF THE INDIRECT EFFECTS OF GUPPIES ON LIFE‐HISTORY EVOLUTION IN RIVULUS HARTII

Early theories of life‐history evolution predict that increased predation on young/small individuals selects for delayed maturation and decreased reproductive effort, but such theory only considers changes in mortality. Predators reduce prey abundance and increase food to survivors. Theory that incorporates such indirect effects yields different predictions. Trinidadian killifish, Rivulus hartii, inhabit communities with and without guppies. Guppies prey on young Rivulus and Rivulus densities decline and growth rates increase when guppies are present. Prior work showed that Rivulus phenotypes from communities with guppies matured earlier and had higher fecundity, consistent with theories that incorporate indirect effects. Here we examined the genetic basis of these differences by rearing 2nd generation, laboratory‐born Rivulus from sites with and without guppies under two food levels that match natural differences in growth. Many locality × food interactions were significant, often reversing the relationship between communities. Such interactions imply that there are fitness trade‐offs associated with adaptation to high or low resource environments. On high food, Rivulus from localities with guppies matured earlier, produced many small eggs, and exhibited increased reproductive investment; these differences reversed on low food. Our results suggest that indirect effects mold Rivulus evolution and thereby highlight connections between community processes and evolutionary change.     

The effects of multiple stressors on wetland communities: pesticides,pathogens and competing amphibians

1. Anthropogenic effects have propelled us into what many have described as the sixth mass extinction, and amphibians are among the most affected groups. The causes of global amphibian population declines and extinctions are varied, complex and context‐dependent and may involve multiple stressors. However, experimental studies examining multiple factors contributing to amphibian population declines are rare. 2. Using outdoor mesocosms containing zooplankton, phytoplankton, periphyton and tadpoles, we conducted a 2 × 2 × 3 factorial experiment that examined the separate and combined effects of an insecticide and the fungal pathogen Batrachochytrium dendrobatidis (Bd) on three different assemblages of larval pacific treefrogs (Pseudacris regilla) and Cascades frogs (Rana cascadae). 3. Larval amphibian growth and development were affected by carbaryl and the amphibian assemblage treatment, but only minimally by Bd. Carbaryl delayed metamorphosis in both amphibian species and increased the growth rate of P. regilla. Carbaryl also reduced cladoceran abundance, which, in turn, had positive effects on phytoplankton abundance but no effect on periphyton biomass. Substituting 20 intraspecific competitors with 20 interspecific competitors decreased the larval period but not the growth rate of P. regilla. In contrast, substituting 20 intraspecific competitors with 20 interspecific competitors had no effect on R. cascadae. Results of real‐time quantitative polymerase chain reaction (qPCR) analysis confirmed infection of Bd‐exposed animals, but exposure to Bd had no effects on either species in univariate analyses, although it had significant or nearly significant effects in several multivariate analyses. In short, we found no interactive effects among the treatments on amphibian growth and development. 4. We encourage future research on the interactive effects of pesticides and pathogens on amphibian communities.     

Female assessment of male functional fertility during mate choice in a promiscuous fish

Sexual selection should favour females that can assess the functional fertility of available sexual partners and avoid mating with recently mated, sperm‐depleted males. Our current understanding of the sensory mechanism(s) underlying female assessment of males based on their functional fertility and avoidance of sperm‐depleted males is incomplete. Female Trinidadian guppies (Poecilia reticulata) are known to avoid mating with males that they had previously observed mating with other females. Here, we investigated experimentally the proximate sensory cues that they use to distinguish between paired size‐ and colour‐matched mated and unmated males in the absence of visual public information on their prior mating histories. When only water‐borne chemical cues from the males were available, females avoided the previously mated male and preferred the unmated one, but they chose randomly when only male visual cues (and no chemical cues) were available. They also preferred unmated over mated males when freely swimming with them in a more sensorially complex environment with multiple male cues (i.e., visual, chemical and mechanical cues) concurrently available. Females exhibited no preference for either stimulus males when both were unmated, irrespectively of the sensory environment. These novel results suggest that, in the absence of prior visual public information on the recent mating histories of males, female guppies use olfactory cues putatively emitted by mated males to avoid mating with them. The source and nature of the implicated olfactory cues and the fitness benefits gained by female guppies in sexually preferring males that have not recently mated remain unknown and warrant further research.     

The cost of males in Daphnia pulex

Sex is paradoxical, because asexuals should replace their sexual ancestors by avoiding the demographic cost of producing males (hereafter referred to as the cost‐of‐males). Despite the large body of theoretical and empirical work dealing with the paradox of sex, the cost‐of‐males assumption has been rarely tested. In the present study, we tested the cost‐of‐males assumption in the cladoceran Daphnia pulex. Populations of this species consist of both cyclically parthenogenetic (i.e. sexuals) and obligately parthenogenetic (i.e. asexuals) lineages. In addition, some of the asexual lineages produce only female offspring, whereas others produce functional males, which can mate with sexual females. We compared the reproductive investment of sexuals, male‐producing asexuals, and non‐male‐producing asexuals when raised separately under various environmental conditions. We also determined the outcome of competition between pair‐wise combinations of these reproductive modes. The cost of males was evident when sexual and asexual females were raised separately: sexuals produced fewer female offspring. However, there was no cost of males when reproductive modes were raised in pairs, as sexuals won the competition with asexuals. Our results directly relate to the field conditions experienced by D. pulex. Sexuals might suffer the cost of males at the beginning of the season, when resource competition is low; but when conditions deteriorate as the population approaches carrying capacity, sexuals seem to be better competitors in spite of male production.     

Predator-induced plasticity in guppy (<Emphasis Type="Italic">Poecilia reticulata</Emphasis>) life history traits

A number of invertebrates show predator-induced plasticity in life-history and morphological traits that are considered adaptive. Evidence is accumulating that vertebrates may also adjust their life-history traits in response to predators; however, some of the patterns of plasticity, which appear to be an adaptive response specifically to the risk of size-selective predation, may instead result from reduced foraging in response to predator presence. Here, we describe a study of predator-induced plasticity in guppies (Poecilia reticulata). We have predicted that the plastic response to cues from a small, gape-limited, natural predator of guppies, the killlifish (Rivulus hartii), would be the opposite of that caused by reduced food intake. We have found that male guppies increased their size at maturity, both length and mass, in response to the non-lethal presence of this predator. This pattern of plasticity is the opposite of that observed in response to reduced food intake, where male guppies reduce size at maturity. The increase in size at maturity that we observed would likely reduce predation on adult male guppies by this native predator because it is gape-limited and can only eat juvenile and small adult guppies. This size advantage would be important especially because male guppies grow very little after maturity. Therefore, the pattern of plasticity that we observed is likely adaptive. In contrast, female guppies showed no significant response in size at first parturition to the experimental manipulation; however, we did find evidence suggesting that females may produce more, smaller offspring in response to cues from this predator.     

Coexistence in the intertidal: interactions between the non‐indigenous New Zealand mud snail Potamopyrgus antipodarum and the native estuarine isopod Gnorimosphaeroma insulare

Nonindigenous species (NIS) that achieve high densities in their recipient communities are expected to have negative effects on native competitors. However, recent reviews have shown that competitors, unlike predators and parasites, have rarely been documented to cause extinctions. There is a need for better understanding of competitive interactions between nonindigenous species and native competitors across systems where NIS reach high densities. In this paper we examine competitive interactions between the exotic, invasive New Zealand mud snail Potamopyrgus antipodarum and native estuarine invertebrates. P. antipodarum is often described as a freshwater snail but can occur in brackish water as well; it has been established in the Columbia River Estuary for over ten years. We addressed competition in this estuarine system using three approaches: field surveys of the benthic invertebrate community, stable isotope analysis of overlap in resource use by common invertebrates, and a laboratory competition experiment that tested the strength of competition between P. antipodarum and the isopod, Gnorimosphaeroma insulare, which overlap in resource use. We found no evidence of negative competitive impacts of P. antipodarum on native benthic invertebrates in this estuarine system. Densities of P. antipodarum and common native epibenthic invertebrates are positively correlated in the intertidal, likely due to shared habitat preferences. The competition experiment showed that the effect of interspecific competition from P. antipodarum on the foraging and survival of G. insulare was significantly less than the effect of intraspecific competition between isopods. The presence of the isopod G. insulare reduced foraging in P. antipodarum, but this change did not result in reduced survival and growth of snails. Hence, interspecific competition is weak despite high densities achieved by the invading species. Finally, we discuss several possible explanations for the observation that P. antipodarum does not have an obvious negative competitive impact on native benthic invertebrates.