Parallel Molecular Evolution in an Herbivore Community

Zhen, Yanan; Aardema, Matthew L.; Medina, Edgar M.; Schumer, Molly; Andolfatto, Peter

doi:10.1126/science.1226630

Cited by 266 publications

(441 citation statements)

References 73 publications

(47 reference statements)

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“…third trophic level) [1,24,35]. Although some specialist herbivores have overcome host defences [42,43], plants are thought to evolve defences in response to multiple herbivores and rates of damage should indicate investment in resistance [16]. While it is possible that alternative evolutionary processes could produce patterns that are consistent with the OU model, for example, fluctuating selection on investment in defence, it is not clear how such processes would result in the observed strong differences in herbivory rates among major plant lineages and on plants with different growth forms.…”

Section: Resultsmentioning

confidence: 99%

Macroecological and macroevolutionary patterns of leaf herbivory across vascular plants

et al. 2014

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The consumption of plants by animals underlies important evolutionary and ecological processes in nature. Arthropod herbivory evolved approximately 415 Ma and the ensuing coevolution between plants and herbivores is credited with generating much of the macroscopic diversity on the Earth. In contemporary ecosystems, herbivory provides the major conduit of energy from primary producers to consumers. Here, we show that when averaged across all major lineages of vascular plants, herbivores consume 5.3% of the leaf tissue produced annually by plants, whereas previous estimates are up to 3.8Â higher. This result suggests that for many plant species, leaf herbivory may play a smaller role in energy and nutrient flow than currently thought. Comparative analyses of a diverse global sample of 1058 species across 2085 populations reveal that models of stabilizing selection best describe rates of leaf consumption, and that rates vary substantially within and among major plant lineages. A key determinant of this variation is plant growth form, where woody plant species experience 64% higher leaf herbivory than non-woody plants. Higher leaf herbivory in woody species supports a key prediction of the plant apparency theory. Our study provides insight into how a long history of coevolution has shaped the ecological and evolutionary relationships between plants and herbivores.

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Section: Resultsmentioning

confidence: 99%

Macroecological and macroevolutionary patterns of leaf herbivory across vascular plants

et al. 2014

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“…Describing widespread parallel evolution on armour plating in wild threespine sticklebacks, Colosimo et al 15 demonstrated the Ectodysplasin signalling pathways to be repeatedly targeted for modifications to this phenotype with a high degree of site-specific parallel evolution. Looking across 14 insect species that feed on cardenolide-producing plants, Zhen et al 45 also noted repeated bouts of parallel evolution for dealing with this toxicity not only confined to the same alpha subunit of the sodium pump (ATPa), but in the great majority of cases to the same two amino acid positions. Examining adaptation to pesticide resistance in Drosophila, four specific point mutations in the Ace gene have been identified, which result in resistance to organophosphates and carbonates (see ref.…”

Section: Box 3 | Expectations and Assumptions Of A Model Of Multiple mentioning

confidence: 99%

On the unfounded enthusiasm for soft selective sweeps

2014

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Underlying any understanding of the mode, tempo and relative importance of the adaptive process in the evolution of natural populations is the notion of whether adaptation is mutation limited. Two very different population genetic models have recently been proposed in which the rate of adaptation is not strongly limited by the rate at which newly arising beneficial mutations enter the population. However, empirical and experimental evidence to date challenges the recent enthusiasm for invoking these models to explain observed patterns of variation in humans and Drosophila.I dentifying the action of positive selection from genomic patterns of variation has remained as a central focus in population genetics. This owes both to the importance of specific applications in fields ranging from ecology to medicine, but also to the desire to address more general evolutionary questions concerning the mode and tempo of adaptation. In this vein, the notion of a soft selective sweep has grown in popularity in the recent literature, and with this increasing usage the definition of the term itself has grown increasingly vague. A soft sweep does not reference a particular population genetic model per se, but rather a set of very different models that may result in similar genomic patterns of variation. Further, it is a term commonly used in juxtaposition with the notion of a hard selective sweep, the classic model in which a single novel beneficial mutation arises in a population and rises in frequency quickly to fixation. Patterns expected under the hard sweep model have been well described in the literature (see reviews of refs 1,2; Box 1), and consist of a reduction in variation surrounding the beneficial mutation owing to the fixation of the single haplotype carrying the beneficial, with resulting well-described skews in the frequency spectrum 3-5 and in patterns of linkage disequilibrium [6][7][8] . Indeed, a part of the recent popularity of soft sweeps comes from the seeming rarity of these expected hard sweep patterns in many natural populations (for example, see refs 9-11).In terms of patterns of variation, the primary difference between soft and hard selective sweeps lies in the expected number of different haplotypes carrying the beneficial mutation or mutations, and thus in the expected number of haplotypes that hitchhike to appreciable frequency during the selective sweep, and which remain in the population at the time of fixation. This key difference results in different expectations in both the site frequency spectrum and in linkage disequilibrium, and thus in the many test statistics based on these patterns (see Box 1). Owing to this ambiguous definition, a number of models have been associated with producing a soft sweep pattern-including selection acting on previously segregating mutations, and multiple beneficials arising via mutation in quick succession (see review ref. 11 and Box 1).

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“…All docking simulations were performed with AutoDock vina 2.0 (55) using an approach similar to that described by Zhen et al (8). To establish a docking protocol we first redocked the cardiac glycoside bufalin into the crystal structure of bufalin bound to the pig Na (27).…”

Section: −7mentioning

confidence: 99%

“…Epitomized by the writings of Gould (5) and Conway Morris (6), this debate centers on whether evolution is stochastic and unpredictable (5) or subject to constraints that limit the available options for evolution, resulting in frequent convergence and a degree of predictability (6). However, evidence of convergence at the genetic level, where similar molecular changes confer the same change in phenotype, is currently limited to only a few taxonomically restricted examples (7)(8)(9)(10)(11).…”

mentioning

confidence: 99%

Widespread convergence in toxin resistance by predictable molecular evolution

Újvári

Casewell

Sunagar

et al. 2015

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

146

183

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The question about whether evolution is unpredictable and stochastic or intermittently constrained along predictable pathways is the subject of a fundamental debate in biology, in which understanding convergent evolution plays a central role. At the molecular level, documented examples of convergence are rare and limited to occurring within specific taxonomic groups. Here we provide evidence of constrained convergent molecular evolution across the metazoan tree of life. We show that resistance to toxic cardiac glycosides produced by plants and bufonid toads is mediated by similar molecular changes to the sodium-potassium-pump (Na + /K + -ATPase) in insects, amphibians, reptiles, and mammals. In toadfeeding reptiles, resistance is conferred by two point mutations that have evolved convergently on four occasions, whereas evidence of a molecular reversal back to the susceptible state in varanid lizards migrating to toad-free areas suggests that toxin resistance is maladaptive in the absence of selection. Importantly, resistance in all taxa is mediated by replacements of 2 of the 12 amino acids comprising the Na + /K + -ATPase H1-H2 extracellular domain that constitutes a core part of the cardiac glycoside binding site. We provide mechanistic insight into the basis of resistance by showing that these alterations perturb the interaction between the cardiac glycoside bufalin and the Na + /K + -ATPase. Thus, similar selection pressures have resulted in convergent evolution of the same molecular solution across the breadth of the animal kingdom, demonstrating how a scarcity of possible solutions to a selective challenge can lead to highly predictable evolutionary responses.constraint | parallelism | genotype phenotype | ion transporters | bufotoxin cardenolide

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Parallel Molecular Evolution in an Herbivore Community

Cited by 266 publications

References 73 publications

Macroecological and macroevolutionary patterns of leaf herbivory across vascular plants

Macroecological and macroevolutionary patterns of leaf herbivory across vascular plants

On the unfounded enthusiasm for soft selective sweeps

Widespread convergence in toxin resistance by predictable molecular evolution

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