Understanding specialism when the jack of all trades can be the master of all

Remold, Susanna K.

doi:10.1098/rspb.2012.1990

Cited by 132 publications

(205 citation statements)

References 70 publications

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“…Not all potential hosts in the host range (different species or different genotypes of the same species) of a virus are equally susceptible to infection, and it is generally assumed that a tight match may exist between host genotypes and virus genotypes to allow a virus to successfully infect a host (6). Indeed, a substantial amount of data supports the idea that by evolving in a single host species or genotype, viruses become specialists (7)(8)(9)(10), whereas by evolving in multiple host species, the result may be no-cost generalists (7,(11)(12)(13).…”

Section: Importancementioning

confidence: 77%

“…Indeed, it has been postulated that pleiotropy is a prerequisite for epistasis (3,40). This dependence is obvious for the case of sign pleiotropy, where mutations with a positive effect in the new host have a negative effect in the primary one (13). Furthermore, in the context of compensatory evolution, antagonistic pleiotropy is a precondition for sign epistasis because it allows for the negative pleiotropic effects of previously selected mutations to be compensated by additional ones (3).…”

Section: Resultsmentioning

confidence: 99%

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Effect of Host Species on Topography of the Fitness Landscape for a Plant RNA Virus

Cervera

Lalić

Elena

2016

J Virol

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Adaptive fitness landscapes are a fundamental concept in evolutionary biology that relate the genotypes of individuals to their fitness. In the end, the evolutionary fate of evolving populations depends on the topography of the landscape, that is, the numbers of accessible mutational pathways and possible fitness peaks (i.e., adaptive solutions). For a long time, fitness landscapes were only theoretical constructions due to a lack of precise information on the mapping between genotypes and phenotypes. In recent years, however, efforts have been devoted to characterizing the properties of empirical fitness landscapes for individual proteins or for microbes adapting to artificial environments. In a previous study, we characterized the properties of the empirical fitness landscape defined by the first five mutations fixed during adaptation of tobacco etch potyvirus (TEV) to a new experimental host, Arabidopsis thaliana. Here we evaluate the topography of this landscape in the ancestral host Nicotiana tabacum. By comparing the topographies of the landscapes for the two hosts, we found that some features remained similar, such as the existence of fitness holes and the prevalence of epistasis, including cases of sign and reciprocal sign epistasis that created rugged, uncorrelated, and highly random topographies. However, we also observed significant differences in the fine-grained details between the two landscapes due to changes in the fitness and epistatic interactions of some genotypes. Our results support the idea that not only fitness tradeoffs between hosts but also topographical incongruences among fitness landscapes in alternative hosts may contribute to virus specialization. IMPORTANCEDespite its importance for understanding virus evolutionary dynamics, very little is known about the topography of virus adaptive fitness landscapes, and even less is known about the effects that different host species and environmental conditions may have on this topography. To bridge this gap, we evaluated the topography of a small fitness landscape formed by all genotypes that result from every possible combination of the first five mutations fixed during adaptation of TEV to the novel host A. thaliana. To assess the effect that host species may have on this topography, we evaluated the fitness of every genotype in both the ancestral and novel hosts. We found that both landscapes share some macroscopic properties, such as the existence of holes and being highly rugged and uncorrelated, yet they differ in microscopic details due to changes in the magnitude and sign of fitness and epistatic effects. T he effects of mutations can be influenced by their interactions with other mutations, with the environment, or both. Epistatic interactions among genetic loci determine the ruggedness of fitness landscapes. In the absence of epistasis, landscapes are single peaked and smooth (1). For such simple landscapes, predicting the result of evolution is an easy task. In contrast, epistatic interactions create curvature in the lands...

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Section: Importancementioning

confidence: 77%

Section: Resultsmentioning

confidence: 99%

Effect of Host Species on Topography of the Fitness Landscape for a Plant RNA Virus

Cervera

Lalić

Elena

2016

J Virol

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“…However, in shaken microcosms that preclude mat formation, WS genotypes cannot invade populations of the SM ancestor from rare (40). These observations show that SM and WS genotypes occupy different niches and coexist due to frequency-dependent fitness interactions and tradeoffs (10,22,34). Coexistence among WS genotypes has also been shown to be stabilized by negative frequency-dependent fitness interactions, indicating differences between their niches (41).…”

Section: Resultsmentioning

confidence: 97%

“…Founder evolvability places an upper limit on the number of organisms with different niches that can emerge by adaptive radiation over an interval of evolutionary time. Moreover, for adaptive radiation to occur, founder evolvability must facilitate generation of diverse niche specialists but preclude "Darwinian demons" with superior, generalist niches that would impede adaptive radiation (10,34). Studies on extant adaptive radiations have begun to probe the impact of evolvability (16,35,36), and its importance for diversification in general is supported by evidence from experimental evolution (e.g., refs.…”

mentioning

confidence: 96%

Founder niche constrains evolutionary adaptive radiation

Flohr

Blom

Rainey

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Adaptive radiation of a lineage into a range of organisms with different niches underpins the evolution of life's diversity. Although the role of the environment in shaping adaptive radiation is well established, theory predicts that the evolvability and niche of the founding ancestor are also of importance. Direct demonstration of a causal link requires resolving the independent effects of these additional factors. Here, we accomplish this using experimental bacterial populations and demonstrate how the dynamics of adaptive radiation are constrained by the niche of the founder. We manipulated the propensity of the founder to undergo adaptive radiation and resolved the underlying causal changes in both its evolvability and niche. Evolvability did not change, but the propensity for adaptive radiation was altered by changes in the position and breadth of the niche of the founder. These observations provide direct empirical evidence for a link between the niche of organisms and their propensity for adaptive radiation. This general mechanism may have rendered the evolutionary dynamics of extant adaptive radiations dependent on chance events that determined their founding ancestors. niche evolution | ecological opportunity | biodiversity

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“…By definition, on any given resource axis, the distribution of the absolute fitness of specialist species is narrow, while generalists have an equal fitness across the axis [1]. It has classically been proposed that 'the jack of all trades is the master of none' [2], which suggests that generalists bear a cost that will reduce their fitness relative to a specialist using the same resource.…”

Section: Introductionmentioning

confidence: 99%

Host specialist clownfishes are environmental niche generalists

2014

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Why generalist and specialist species coexist in nature is a question that has interested evolutionary biologists for a long time. While the coexistence of specialists and generalists exploiting resources on a single ecological dimension has been theoretically and empirically explored, biological systems with multiple resource dimensions (e.g. trophic, ecological) are less well understood. Yet, such systems may provide an alternative to the classical theory of stable evolutionary coexistence of generalist and specialist species on a single resource dimension. We explore such systems and the potential tradeoffs between different resource dimensions in clownfishes. All species of this iconic clade are obligate mutualists with sea anemones yet show interspecific variation in anemone host specificity. Moreover, clownfishes developed variable environmental specialization across their distribution. In this study, we test for the existence of a relationship between host-specificity (number of anemones associated with a clownfish species) and environmental-specificity (expressed as the size of the ecological niche breadth across climatic gradients). We find a negative correlation between host range and environmental specificities in temperature, salinity and pH, probably indicating a trade-off between both types of specialization forcing species to specialize only in a single direction. Trade-offs in a multi-dimensional resource space could be a novel way of explaining the coexistence of generalist and specialists.

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Understanding specialism when the jack of all trades can be the master of all

Cited by 132 publications

References 70 publications

Effect of Host Species on Topography of the Fitness Landscape for a Plant RNA Virus

Effect of Host Species on Topography of the Fitness Landscape for a Plant RNA Virus

Founder niche constrains evolutionary adaptive radiation

Host specialist clownfishes are environmental niche generalists

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