An official website of the United States government
There is increasing evidence that genetic evolution can occur rapidly enough to affect the ecological dynamics of populations and communities ( 1 – 3 ). To better predict the future of ecosystems, it is necessary to understand how evolutionary changes within species influence and interact with ecological changes through processes known as “eco-evolutionary dynamics” ( 4 ). On page 70 of this issue, Barbour et al. ( 5 ) demonstrate that a gene affecting a plant’s resistance to herbivory also influences the persistence of the food web through the gene’s effect on plant growth (see the figure). Subsequent studies of natural selection in the wild can help explain how variations of such “keystone genes” can be maintained ( 6 , 7 ). The maintenance of genetic variation in keystone genes is required for eco-evolutionary dynamics to be perpetual rather than transient.
more »
« less
Dispersal stabilizes coupled ecological and evolutionary dynamics in a host-parasitoid system
When ecological and evolutionary dynamics occur on comparable timescales, persistence of the ensuing eco-evolutionary dynamics requires both ecological and evolutionary stability. This unites key questions in ecology and evolution: How do species coexist, and what maintains genetic variation in a population? In this work, we investigated a host-parasitoid system in which pea aphid hosts rapidly evolve resistance toAphidius erviparasitoids. Field data and mathematical simulations showed that heterogeneity in parasitoid dispersal can generate variation in parasitism-mediated selection on hosts through time and space. Experiments showed how evolutionary trade-offs plus moderate host dispersal across this selection mosaic cause host-parasitoid coexistence and maintenance of genetic variation in host resistance. Our results show how dispersal can stabilize both the ecological and evolutionary components of eco-evolutionary dynamics.
more »
« less
- Award ID(s):
- 1240892
- PAR ID:
- 10612402
- Publisher / Repository:
- American Association for the Advancement of Science
- Date Published:
- Journal Name:
- Science
- Volume:
- 383
- Issue:
- 6688
- ISSN:
- 0036-8075
- Page Range / eLocation ID:
- 1240 to 1244
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Viruses and their hosts can undergo coevolutionary arms races where hosts evolve increased resistance and viruses evolve counter‐resistance. Given these arms race dynamics (ARD), both players are predicted to evolve along a single trajectory as more recently evolved genotypes replace their predecessors. By coupling phenotypic and genomic analyses of coevolving populations of bacteriophageλandEscherichia coli, we find conflicting evidence for ARD. Virus‐host infection phenotypes fit the ARD model, yet genomic analyses revealed fluctuating selection dynamics. Rather than coevolution unfolding along a single trajectory, cryptic genetic variation emerges and is maintained at low frequency for generations until it eventually supplants dominant lineages. These observations suggest a hybrid ‘leapfrog’ dynamic, revealing weaknesses in the predictive power of standard coevolutionary models. The findings shed light on the mechanisms that structure coevolving ecological networks and reveal the limits of using phenotypic or genomic data alone to differentiate coevolutionary dynamics.more » « less
-
Abstract Host–parasite interactions may often be subject to opposing evolutionary forces, which likely influence the evolutionary trajectories of both partners. Natural selection and genetic drift are two major evolutionary forces that act in host and parasite populations. Further, population size is a significant determinant of the relative strengths of these forces. In small populations, drift may undermine the persistence of beneficial alleles, potentially impeding host adaptation to parasites. Here, we investigate two questions: (a) can selection pressure for increased resistance in small, susceptible host populations overcome the effects of drift and (b) can resistance be maintained in small host populations? To answer these questions, we experimentally evolved the hostCaenorhabditis elegansagainst its bacterial parasite,Serratia marcescens, for 13 host generations. We found that strong selection favouring increased host resistance was insufficient to counteract drift in small populations, resulting in persistently high host mortality. Additionally, in small populations of resistant hosts, we found that selection for the maintenance of resistance is not always sufficient to curb the loss of resistance. We compared these results with selection in large host populations. We found that initially resistant, large host populations were able to maintain high levels of resistance. Likewise, initially susceptible, large host populations were able to gain resistance to the parasite. These results show that strong selection pressure for survival is not always sufficient to counteract drift. In consideration ofC.elegans natural population dynamics, we suggest that drift may often impede selection in nature.more » « less
-
Abstract Juveniles are typically less resistant (more susceptible) to infectious disease than adults, and this difference in susceptibility can help fuel the spread of pathogens in age‐structured populations. However, evolutionary explanations for this variation in resistance across age remain to be tested.One hypothesis is that natural selection has optimized resistance to peak at ages where disease exposure is greatest. A central assumption of this hypothesis is that hosts have the capacity to evolve resistance independently at different ages. This would mean that host populations have (a) standing genetic variation in resistance at both juvenile and adult stages, and (b) that this variation is not strongly correlated between age classes so that selection acting at one age does not produce a correlated response at the other age.Here we evaluated the capacity of three wild plant species (Silene latifolia,S. vulgarisandDianthus pavonius) to evolve resistance to their anther‐smut pathogens (Microbotryumfungi), independently at different ages. The pathogen is pollinator transmitted, and thus exposure risk is considered to be highest at the adult flowering stage.Within each species we grew families to different ages, inoculated individuals with anther smut, and evaluated the effects of age, family and their interaction on infection.In two of the plant species,S. latifoliaandD. pavonius, resistance to smut at the juvenile stage was not correlated with resistance to smut at the adult stage. In all three species, we show there are significant age × family interaction effects, indicating that age specificity of resistance varies among the plant families.Synthesis. These results indicate that different mechanisms likely underlie resistance at juvenile and adult stages and support the hypothesis that resistance can evolve independently in response to differing selection pressures as hosts age. Taken together our results provide new insight into the structure of genetic variation in age‐dependent resistance in three well‐studied wild host–pathogen systems.more » « less
-
Theory often predicts that host populations should evolve greater resistance when parasites become abundant. Furthermore, that evolutionary response could ameliorate declines in host populations during epidemics. Here, we argue for an update: when all host genotypes become sufficiently infected, higher parasite abundance can select for lower resistance because its cost exceeds its benefit. We illustrate such a “resistance is futile” outcome with mathematical and empirical approaches. First, we analyzed an eco-evolutionary model of parasites, hosts, and hosts’ resources. We determined eco-evolutionary outcomes for prevalence, host density, and resistance (mathematically, “transmission rate”) along ecological and trait gradients that alter parasite abundance. With high enough parasite abundance, hosts evolve lower resistance, amplifying infection prevalence and decreasing host density. In support of these results, a higher supply of nutrients drove larger epidemics of survival-reducing fungal parasites in a mesocosm experiment. In two-genotype treatments, zooplankton hosts evolved less resistance under high-nutrient conditions than under low-nutrient conditions. Less resistance, in turn, was associated with higher infection prevalence and lower host density. Finally, in an analysis of naturally occurring epidemics, we found a broad, bimodal distribution of epidemic sizes consistent with the resistance is futile prediction of the eco-evolutionary model. Together, the model and experiment, supplemented by the field pattern, support predictions that drivers of high parasite abundance can lead to the evolution of lower resistance. Hence, under certain conditions, the most fit strategy for individual hosts exacerbates prevalence and depresses host populations.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1126/science.adg4602
