Diverse,endemic and polyphyletic clones in mixed populations of a freshwater snail (Potamopyrgus antipodarum)

Understanding the source and diversity of clones is necessary to resolve the complicated issues surrounding the apparent evolutionary stability of sexual reproduction. The source of clones is important because present theory is based on an “all else equal” assumption, which is predicated on the idea that clonal mutants are derived from and compete with local sexual populations. Clonal diversity is important because it reduces the advantage of sexual reproduction under either soft selection (the Tangled Bank Hypothesis) or under strict frequency-dependent selection (the Red Queen Hypothesis). In the present study, protein electrophoresis was used to determine the source and diversity of clones in a freshwater snail (Potamopyrgus antipodarum) in four glacial lakes in which sexual and clonal females were thought to coexist. The results showed (1) that the populations were mixtures of diploid sexual and triploid asexual individuals, (2) that genotypic diversity of clonal populations is very high in all four lakes (but lower than in the sympatric sexual populations), and (3) that the clones are polyphyletically derived from their sympatric sexual populations. Consequently, repeated mutation to parthenogenetic reproduction since the Pleistocene has introduced a different and diverse set of clones in all four lakes. Such diversity may provide a challenge for the ecological theories of sex that rely on frequency-dependent selection.     

The Ratchet and the Red Queen: the maintenance of sex in parasites

The adaptive significance of sexual reproduction remains as an unsolved problem in evolutionary biology. One promising hypothesis is that frequency‐dependent selection by parasites selects for sexual reproduction in hosts, but it is unclear whether such selection on hosts would feed back to select for sexual reproduction in parasites. Here we used individual‐based computer simulations to explore this possibility. Specifically, we tracked the dynamics of asexual parasites following their introduction into sexual parasite populations for different combinations of parasite virulence and transmission. Our results suggest that coevolutionary interactions with hosts would generally lead to a stable coexistence between sexual parasites and a single parasite clone. However, if multiple mutations to asexual reproduction were allowed, we found that the interaction led to the accumulation of clonal diversity in the asexual parasite population, which led to the eventual extinction of the sexual parasites. Thus, coevolution with sexual hosts may not be generally sufficient to select for sex in parasites. We then allowed for the stochastic accumulation of mutations in the finite parasite populations (Muller's Ratchet). We found that, for higher levels of parasite virulence and transmission, the population bottlenecks resulting from host–parasite coevolution led to the rapid accumulation of mutations in the clonal parasites and their elimination from the population. This result may explain the observation that sexual reproduction is more common in parasitic animals than in their free‐living relatives.     

Running with the Red Queen: the role of biotic conflicts in evolution

What are the causes of natural selection? Over 40 years ago, Van Valen proposed the Red Queen hypothesis, which emphasized the primacy of biotic conflict over abiotic forces in driving selection. Species must continually evolve to survive in the face of their evolving enemies, yet on average their fitness remains unchanged. We define three modes of Red Queen coevolution to unify both fluctuating and directional selection within the Red Queen framework. Empirical evidence from natural interspecific antagonisms provides support for each of these modes of coevolution and suggests that they often operate simultaneously. We argue that understanding the evolutionary forces associated with interspecific interactions requires incorporation of a community framework, in which new interactions occur frequently. During their early phases, these newly established interactions are likely to drive fast evolution of both parties. We further argue that a more complete synthesis of Red Queen forces requires incorporation of the evolutionary conflicts within species that arise from sexual reproduction. Reciprocally, taking the Red Queen''s perspective advances our understanding of the evolution of these intraspecific conflicts.     

PREY ADAPTATION AS A CAUSE OF PREDATOR-PREY CYCLES

We analyze simple models of predator-prey systems in which there is adaptive change in a trait of the prey that determines the rate at which it is captured by searching predators. Two models of adaptive change are explored: (1) change within a single reproducing prey population that has genetic variation for vulnerability to capture by the predator; and (2) direct competition between two independently reproducing prey populations that differ in their vulnerability. When an individual predator's consumption increases at a decreasing rate with prey availability, prey adaptation via either of these mechanisms may produce sustained cycles in both species' population densities and in the prey's mean trait value. Sufficiently rapid adaptive change (e.g., behavioral adaptation or evolution of traits with a large additive genetic variance), or sufficiently low predator birth and death rates will produce sustained cycles or chaos, even when the predator-prey dynamics with fixed prey capture rates would have been stable. Adaptive dynamics can also stabilize a system that would exhibit limit cycles if traits were fixed at their equilibrium values. When evolution fails to stabilize inherently unstable population interactions, selection decreases the prey's escape ability, which further destabilizes population dynamics. When the predator has a linear functional response, evolution of prey vulnerability always promotes stability. The relevance of these results to observed predator-prey cycles is discussed.     

Effects of risk, cost, and their interaction on optimal escape by nonrefuging Bonaire whiptail lizards, Cnemidophorus murinus

Optimal escape theory seeks to explain variation in the distanceto an approaching predator at which the prey initiates escape(flight initiation distance). Flight initiation distance increaseswhen predators pose a greater threat and decreases when escapecosts increase. Although optimal escape theory has been highlysuccessful, its predictions have been tested primarily for speciesthat escape to discrete refuges, and most studies have focusedon single risk or cost factors. We present data from two experimentsin which two risks or a risk and a cost varied in Bonaire whiptaillizards (Cnemidophorus murinus) that escaped without enteringrefuges. Our data verify several predictions about optimal escapefor nonrefuging lizard prey. Two risk factors, speed and directnessof approach by the predator, interacted. Directly approachedlizards had greater flight initiation distances than did indirectlyapproached lizards when approached rapidly, but shorter flightinitiation distances when approached slowly. Flight initiationdistance was shorter in the presence of food and during slowversus rapid approaches, but contrary to expectation, food presenceand approach speed did not interact. This would be explainedif cost curves are nonlinear or if they are parallel ratherthan intersecting when the predator reaches the prey. More empiricalwork is needed to determine which risk and cost factors actadditively and which act synergistically. The absence of interactionbetween the risk and cost factors suggests that cost curveswere nonlinear.     

Empirical studies of escape behavior find mixed support for the race for life model

Escape theory has been exceptionally successful in conceptualizing and accurately predicting effects of numerous factors that affect predation risk and explaining variation in flight initiation distance (FID; predator–prey distance when escape begins). Less explored is the relative orientation of an approaching predator, prey, and its eventual refuge. The relationship between an approaching threat and its refuge can be expressed as an angle we call the “interpath angle” or “Φ,” which describes the angle between the paths of predator and prey to the prey’s refuge and thus expresses the degree to which prey must run toward an approaching predator. In general, we might expect that prey would escape at greater distances if they must flee toward a predator to reach its burrow. The “race for life” model makes formal predictions about how Φ should affect FID. We evaluated the model by studying escape decisions in yellow-bellied marmots Marmota flaviventer, a species which flees to burrows. We found support for some of the model’s predictions, yet the relationship between Φ and FID was less clear. Marmots may not assess Φ in a continuous fashion; but we found that binning angle into 4 45° bins explained a similar amount of variation as models that analyzed angle continuously. Future studies of Φ, especially those that focus on how different species perceive relative orientation, will likely enhance our understanding of its importance in flight decisions.     

Recombination in a Simulated Predator-Prey Interaction

The influence of a co-evolved predator-prey interaction on theoutcome of competition between sexual and asexual prey was examinedby computer simulation. Intraspecific competition in both predatorand prey populations is governed by relative success in theinterspecific interaction. Predators key on a certain variableprey character under the control often independently assorting,diploid loci. Individual predators vary genetically in theirability to handle prey of the various states of this character.Predator fitness is proportional to the prey available to them.Prey fitness is inversely proportional to the frequency of predatorsto which they are susceptible. In addition, sexual prey of agiven phenotype are assigned half the fitness of the correspondingasexual form, representing a "cost of meiosis." Mating is randomand there is no facultative response allowed to changes in thephenotypic distribution of the interacting species. Three parametersare varied: (1) the maximum contribution of a phenotype to thenext generation (fecundity limit), (2) population size, and(3) clonal diversity of the asexual prey form. Most realisticcombinations of these variables favor sexual reproduction. Accordingto the model, it is particularly unlikely that an asexual mutantcould spread in an existing sexual population. However, theconditions found to favor asexuality are consistent with observationsfrom nature where reduced recombination is relatively common.The model predicts asexual forms should persist in very large,low fecund populations, as in the prokaryotes, and where theirphenotypic diversity is high, as near zones of recurrent hybridization.It is also consistent with the occurrence of parthenoforms inregions of reduced interspecific interaction where the assumptionsof this model, and therefore the advantages to sex, are lesslikely to be realized.     

Thermal acclimation of interactions: differential responses to temperature change alter predator-prey relationship

Different species respond differently to environmental change so that species interactions cannot be predicted from single-species performance curves. We tested the hypothesis that interspecific difference in the capacity for thermal acclimation modulates predator-prey interactions. Acclimation of locomotor performance in a predator (Australian bass, Macquaria novemaculeata) was qualitatively different to that of its prey (eastern mosquitofish, Gambusia holbrooki). Warm (25°C) acclimated bass made more attacks than cold (15°C) acclimated fish regardless of acute test temperatures (10-30°C), and greater frequency of attacks was associated with increased prey capture success. However, the number of attacks declined at the highest test temperature (30°C). Interestingly, escape speeds of mosquitofish during predation trials were greater than burst speeds measured in a swimming arena, whereas attack speeds of bass were lower than burst speeds. As a result, escape speeds of mosquitofish were greater at warm temperatures (25°C and 30°C) than attack speeds of bass. The decline in the number of attacks and the increase in escape speed of prey means that predation pressure decreases at high temperatures. We show that differential thermal responses affect species interactions even at temperatures that are within thermal tolerance ranges. This thermal sensitivity of predator-prey interactions can be a mechanism by which global warming affects ecological communities.     

Host-parasite coevolution induces selection for condition-dependent sex

Sex and recombination remain one of the biggest riddles of evolutionary biology. One of the most prominent hypotheses, the Red Queen Hypothesis, claims that sex has evolved as a means to efficiently create genotypes that are resistant against coevolving parasites. However, previous models of the Red Queen have assumed that all individuals are equally likely to engage in sexual reproduction, regardless of their infection status, an assumption that may not be true in reality. Here, we consider a population genetic model of a host population coevolving with a parasite population, where the parasites are haploid and the hosts either haploid or diploid. We assume that the probability to engage in sex may be different in infected and uninfected hosts and ascertain the success of different reproductive strategies with a modifier-gene approach. Our model shows that in the large majority of the parameter space, infection-dependent sex is more successful than infection-independent sex. We identify at least two reasons for this: (i) an immediate short-term advantage of breaking-down gene combinations of unfit individuals and (ii) a selfish spread of the condition-dependent modifiers, in analogy to the 'abandon-ship' effect in single species. In diploids, these effects are often powerful enough to overcome the detrimental effects of segregation. These results raise the intriguing question of why infection-induced sex is not more commonly observed in nature.     

An emerging infectious disease triggering large-scale hyperpredation

Hyperpredation refers to an enhanced predation pressure on a secondary prey due to either an increase in the abundance of a predator population or a sudden drop in the abundance of the main prey. This scarcely documented mechanism has been previously studied in scenarios in which the introduction of a feral prey caused overexploitation of native prey. Here we provide evidence of a previously unreported link between Emergent Infectious Diseases (EIDs) and hyperpredation on a predator-prey community. We show how a viral outbreak caused the population collapse of a host prey at a large spatial scale, which subsequently promoted higher-than-normal predation intensity on a second prey from shared predators. Thus, the disease left a population dynamic fingerprint both in the primary host prey, through direct mortality from the disease, and indirectly in the secondary prey, through hyperpredation. This resulted in synchronized prey population dynamics at a large spatio-temporal scale. We therefore provide evidence for a novel mechanism by which EIDs can disrupt a predator-prey interaction from the individual behavior to the population dynamics. This mechanism can pose a further threat to biodiversity through the human-aided disruption of ecological interactions at large spatial and temporal scales.     

The role of epistasis on the evolution of recombination in host-parasite coevolution

Antagonistic coevolution between hosts and parasites is known to affect selection on recombination in hosts. The Red Queen Hypothesis (RQH) posits that genetic shuffling is beneficial for hosts because it quickly creates resistant genotypes. Indeed, a large body of theoretical studies have shown that for many models of the genetic interaction between host and parasite, the coevolutionary dynamics of hosts and parasites generate selection for recombination or sexual reproduction. Here we investigate models in which the effect of the host on the parasite (and vice versa) depend approximately multiplicatively on the number of matched alleles. Contrary to expectation, these models generate a dynamical behavior that strongly selects against recombination/sex. We investigate this atypical behavior analytically and numerically. Specifically we show that two complementary equilibria are responsible for generating strong linkage disequilibria of opposite sign, which in turn causes strong selection against sex. The biological relevance of this finding stems from the fact that these phenomena can also be observed if hosts are attacked by two parasites that affect host fitness independently. Hence the role of the Red Queen Hypothesis in natural host parasite systems where infection by multiple parasites is the rule rather than the exception needs to be reevaluated.     

Evidence for the Predator Attraction Hypothesis in an amphibian predator–prey system

Many species possess damage-released chemical alarm cues that function in alerting nearby individuals to a predator attack. One hypothesis for the evolution and/or maintenance of such cues is the Predator Attraction Hypothesis, where predators, rather than prey, are the “intended” recipients of these cues. If a predator attack attracts additional predators, these secondary predators might interfere with the predation event, providing the prey with a better chance to escape. In this study, we conducted two experiments to explore this hypothesis in an amphibian predator/prey system. In Experiment 1, we found that tiger salamanders (Ambystoma mavortium) showed a foraging attraction to chemical cues from wood frog (Lithobates sylvaticus) tadpoles. Salamanders that were experienced with tadpole prey, in particular, were strongly attracted to tadpole alarm cues. In Experiment 2, we observed experimental encounters between a tadpole and either one or two salamanders. The presence of the second predator caused salamanders to increase attack speed at the cost of decreased attack accuracy (i.e., increasing the probability that the tadpole would escape attacks). We also found that the mere presence of visual and chemical cues from a second predator did not affect this speed/accuracy trade-off but did cause enough of a distraction to increase tadpole survival. Thus, our findings are consistent with the Predator Attraction Hypothesis for the evolution and/or maintenance of alarm cues.     

The maintenance of sex: host–parasite coevolution with density‐dependent virulence

Why don’t asexual females replace sexual females in most natural populations of eukaryotes? One promising explanation is that parasites could counter the reproductive advantages of asexual reproduction by exerting frequency‐dependent selection against common clones (the Red Queen hypothesis). One apparent limitation of the Red Queen theory, however, is that parasites would seem to be required by theory to be highly virulent. In the present study, I present a population‐dynamic view of competition between sexual females and asexual females that interact with co‐evolving parasites. The results show that asexual populations have higher carrying capacities, and more unstable population dynamics, than sexual populations. The results also suggest that the spread of a clone into a sexual population could increase the effective parasite virulence as population density increases. This combination of parasite‐mediated frequency‐dependent selection, and density‐dependent virulence, could lead to the coexistence of sexual and asexual reproductive strategies and the long‐term persistence of sex.     

Predator-prey dynamics and movement in fractal environments

Previous research suggests that local interactions and limited animal mobility can affect population dynamics. However, the spatial structure of the environment can further limit the mobility of animals. For example, an animal confined to a river valley or to a particular plant cannot move with equal ease in all directions. We show that spatial architecture could influence the population dynamics of predator-prey systems using individual-based computer simulations parameterized with allometric relationships from the literature. Spatial forms (representing geographical features or plant architecture) of differing fractal dimension were generated, and simulated predators and prey were introduced into these computer environments. We claim that the alteration in interaction rates and population dynamics found in these simulations can be explained as a consequence of the anomalously slow rates of movement associated with fractal spaces and the diffusion-limited nature of predator-prey interactions. As a result, functional responses and numerical responses are substantially reduced in fractal environments, and the overall stability of the system is determined by the interaction between individual mobility and spatial architecture.     

Eco‐evolutionary feedback promotes Red Queen dynamics and selects for sex in predator populations

Although numerous hypotheses exist to explain the overwhelming presence of sexual reproduction across the tree of life, we still cannot explain its prevalence when considering all inherent costs involved. The Red Queen hypothesis states that sex is maintained because it can create novel genotypes with a selective advantage. This occurs when the interactions between species induce frequent environmental change. Here, we investigate whether coevolution and eco‐evolutionary feedback dynamics in a predator‐prey system allows for indirect selection and maintenance of sexual reproduction in the predator. Combining models and chemostat experiments of a rotifer‐algae system we show a continuous feedback between population and trait change along with recurrent shifts from selection by predation and competition for a limited resource. We found that a high propensity for sex was indirectly selected and was maintained in rotifer populations within environments containing these eco‐evolutionary dynamics; whereas within environments under constant conditions, predators evolved rapidly to lower levels of sex. Thus, our results indicate that the influence of eco‐evolutionary feedback dynamics on the overall evolutionary change has been underestimated.     

Strategic Escape Direction: Orientation,Turning, and Escape Trajectories of Zebra‐Tailed Lizards (Callisaurus draconoides)

A prey's body orientation relative to a predator's approach path may affect risk of fleeing straight ahead. Consequently, prey often turn before fleeing. Relationships among orientation, turn, and escape angles and between these angles and predation risk have not been studied in terrestrial vertebrates and have rarely been studied in the field. Escape angles are expected to lead away from predators and be highly variable to avoid being predictable by predators. Using approach speed as a risk factor, we studied these issues in the zebra‐tailed lizard, Callisaurus draconoides. Lizards fled away from human simulated predators, but most did not flee straight away. Escape angles were variable, as expected under the unpredictability hypothesis, and had modes at nearly straight away (i.e., 0°) and nearly perpendicular to the predator's approach path (90°). The straight away mode suggests maximal distancing from the predator; the other mode suggests maintaining ability to monitor the predator or possibly an influence of habitat features such as obstacles and refuges that differ among directions. Turn angles were larger when orientation was more toward the predator, and escape angles were closer to straight away when turn angles were larger. Turning serves to reach a favorable fleeing direction. When orientation angle was more toward the predator, escape angle was unaffected, suggesting that turn angle compensates completely for increased risk of orientation toward the predator. When approached more rapidly, lizards fled more nearly straight away, as expected under greater predation risk. Turn angles were unrelated to approach speed.     

Red Queen dancing in the lek: effects of mating skew on host–parasite interactions

The RQH (Red Queen hypothesis), which argues that hosts need to be continuously finding new ways to avoid parasites that are able to infect common host genotypes, has been at the center of discussions on the maintenance of sex. This is because diversity is favored under the host–parasite coevolution based on negative frequency‐dependent selection, and sexual reproduction is a mechanism that generates genetic diversity in the host population. Together with parasite infections, sexual organisms are usually under sexual selection, which leads to mating skew or mating success biased toward males with a particular phenotype. Thus, strong mating skew would affect genetic variance in a population and should affect the benefit of the RQH. However, most models have investigated the RQH under a random mating system and not under mating skew. In this study, I show that sexual selection and the resultant mating skew may increase parasite load in the hosts. An IBM (individual‐based model), which included host–parasite interactions and sexual selection among hosts, demonstrates that mating skew influenced parasite infection in the hosts under various conditions. Moreover, the IBM showed that the mating skew evolves easily in cases of male–male competition and female mate choice, even though it imposes an increased risk of parasite infection on the hosts. These findings indicated that whether the RQH favored sexual reproduction depended on the condition of mating skew. That is, consideration of the host mating system would provide further understanding of conditions in which the RQH favors sexual reproduction in real organisms.     

Responses of a carnivorous plant to prey and inorganic nutrients in a Mediterranean environment

We have analysed the effect of prey and fertilization by inorganic nutrients on the survival, growth, reproduction (sexual and vegetative) and mucilage secretion of Pinguicula vallisneriifolia (Lentibulariaceae), a carnivorous plant inhabiting rocky substrates of southern Spain. We tested the hypothesis that carnivorous plants are more prey dependent when root access to nutrients is strongly limited by (1) analysing the importance of the carnivorous habit to the fitness of P. vallisneriifolia in its natural rocky habitat, and (2) determining whether the effect of trapped prey varies with soil nutrient levels. Our 2-year experimental results indicated prey to be limiting to P. vallisneriifolia growth on its natural rocky substrate. Animal food supply substantially increased the chance of survival, growth, vegetative propagation, sexual reproductive success and mucilage secretion. The differences between prey levels were more evident at the end of the experiment when all the surviving Prey-exclusion plants had lost weight, and the probability of sexual reproduction and of vegetative propagation by axillary buds had accordingly diminished. Furthermore, there were clear benefits from carnivory at the population level, since both the expected individual life span and the lifetime vegetative and sexual output correlated positively with the quantity of prey trapped. Application of insects to non-fertilized plants stimulated growth, but similar application to fertilized plants grown on a complete nutrient solution failed to enhance growth. There was no obvious benefit from the provision of a balanced mineral nutrient solution (alone or with prey). The greatest absolute growth and sexual and vegetative output resulted from providing a surplus of insects to plants on their natural rocky substrate. The strong dependence of P. vallisneriifolia on prey can therefore be considered a useful preadaptation enabling colonization of rocky substrates. Received: 11 November 1996 / Accepted: 31 March 1997     

Antagonistic species interaction drives selection for sex in a predator–prey system

The evolutionary maintenance of sexual reproduction has long challenged biologists as the majority of species reproduce sexually despite inherent costs. Providing a general explanation for the evolutionary success of sex has thus proven difficult and resulted in numerous hypotheses. A leading hypothesis suggests that antagonistic species interaction can generate conditions selecting for increased sex due to the production of rare or novel genotypes that are beneficial for rapid adaptation to recurrent environmental change brought on by antagonism. To test this ecology‐based hypothesis, we conducted experimental evolution in a predator (rotifer)–prey (algal) system by using continuous cultures to track predator–prey dynamics and in situ rates of sex in the prey over time and within replicated experimental populations. Overall, we found that predator‐mediated fluctuating selection for competitive versus defended prey resulted in higher rates of genetic mixing in the prey. More specifically, our results showed that fluctuating population sizes of predator and prey, coupled with a trade‐off in the prey, drove the sort of recurrent environmental change that could provide a benefit to sex in the prey, despite inherent costs. We end with a discussion of potential population genetic mechanisms underlying increased selection for sex in this system, based on our application of a general theoretical framework for measuring the effects of sex over time, and interpreting how these effects can lead to inferences about the conditions selecting for or against sexual reproduction in a system with antagonistic species interaction.     

The effect of spatial heterogeneity on the persistence of predator-prey interactions

The effect of spatially discontinuous environments on predator-prey systems is examined by using a computer simulation model. It is shown that increasing prey dispersal and decreasing predator dispersal do not necessarily have a stabilizing influence on the interaction, as had been concluded by previous workers. The stability of predator-prey interaction depends on the interaction of the dispersal process with normal reproduction and feeding of the predator and prey species.