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Genetic drift precluded adaptation of an insect seed predator to a novel host plant in a long-term selection experiment.

ABSTRACT: Host specialization is considered a primary driver of the enormous diversity of herbivorous insects. Trade-offs in host use are hypothesized to promote this specialization, but they have mostly been studied in generalist herbivores. We conducted a multi-generation selection experiment to examine the adaptation of the specialist seed-feeding bug, Lygaeus equestris, to three novel host plants (Helianthus annuus, Verbascum thapsus and Centaurea phrygia) and to test whether trade-offs promote specialization. During the selection experiment, body size of L. equestris increased more on the novel host plant H. annuus compared to the primary host plant, Vincetoxicum hirundinaria, but this effect was not observed in other fitness related traits. In addition to selection, genetic drift caused variation among the experimental herbivore populations in their ability to exploit the host plants. Microsatellite data indicated that the level of within-population genetic variation decreased and population differentiation increased more in the selection line feeding on H. annuus compared to V. hirundinaria. We found a negative correlation between genetic differentiation and heterozygosity at the end of the experiment, suggesting that differentiation was significantly affected by genetic drift. We did not find fitness trade-offs between L. equestris feeding on the four hosts. Thus, trade-offs do not seem to promote specialization in L. equestris. Our results suggest that this insect herbivore is not likely to adapt to a novel host species in a time-scale of 20 generations despite sufficient genetic variation and that genetic drift disrupted the response to selection.

SUBMITTER: Laukkanen L

PROVIDER: S-EPMC5997315 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Genetic drift precluded adaptation of an insect seed predator to a novel host plant in a long-term selection experiment.

Laukkanen Liisa L Kalske Aino A Muola Anne A Leimu Roosa R Mutikainen Pia P

PloS one 20180612 6

Host specialization is considered a primary driver of the enormous diversity of herbivorous insects. Trade-offs in host use are hypothesized to promote this specialization, but they have mostly been studied in generalist herbivores. We conducted a multi-generation selection experiment to examine the adaptation of the specialist seed-feeding bug, Lygaeus equestris, to three novel host plants (Helianthus annuus, Verbascum thapsus and Centaurea phrygia) and to test whether trade-offs promote specia ...[more]

PMID: 29894503

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Project description:Manipulating evolutionary forces imposed by hosts on pathogens like genetic drift and selection could avoid the emergence of virulent pathogens. For instance, increasing genetic drift could decrease the risk of pathogen adaptation through the random fixation of deleterious mutations or the elimination of favorable ones in the pathogen population. However, no experimental proof of this approach is available for a plant-pathogen system. We studied the impact of pepper (Capsicum annuum) lines carrying the same major resistance gene but contrasted genetic backgrounds on the evolution of Potato virus Y (PVY). The pepper lines were chosen for the contrasted levels of genetic drift (inversely related to Ne, the effective population size) they exert on PVY populations, as well as for their contrasted resistance efficiency (inversely related to the initial replicative fitness, Wi, of PVY in these lines). Experimental evolution was performed by serially passaging 64 PVY populations every month on six contrasted pepper lines during seven months. These PVY populations exhibited highly divergent evolutionary trajectories, ranging from viral extinctions to replicative fitness gains. The sequencing of the PVY VPg cistron, where adaptive mutations are likely to occur, allowed linking these replicative fitness gains to parallel adaptive nonsynonymous mutations. Evolutionary trajectories were well explained by the genetic drift imposed by the host. More specifically, Ne, Wi and their synergistic interaction played a major role in the fate of PVY populations. When Ne was low (i.e. strong genetic drift), the final PVY replicative fitness remained close to the initial replicative fitness, whereas when Ne was high (i.e. low genetic drift), the final PVY replicative fitness was high independently of the replicative fitness of the initially inoculated virus. We show that combining a high resistance efficiency (low Wi) and a strong genetic drift (low Ne) is the best solution to increase resistance durability, that is, to avoid virus adaptation on the long term.

Project description:Long-term biodiversity experiments have shown increasing strengths of biodiversity effects on plant productivity over time. However, little is known about rapid evolutionary processes in response to plant community diversity, which could contribute to explaining the strengthening positive relationship. To address this issue, we performed a transplant experiment with offspring of seeds collected from four grass species in a 14-year-old biodiversity experiment (Jena Experiment). We used two- and six-species communities and removed the vegetation of the study plots to exclude plant-plant interactions. In a reciprocal design, we transplanted five "home" phytometers (same origin and actual environment), five "away-same" phytometers (same species richness of origin and actual environment, but different plant composition), and five "away-different" phytometers (different species richness of origin and actual environment) of the same species in the study plots. In the establishment year, plants transplanted in home soil produced more shoots than plants in away soil indicating that plant populations at low and high diversity developed differently over time depending on their associated soil community and/or conditions. In the second year, offspring of individuals selected at high diversity generally had a higher performance (biomass production and fitness) than offspring of individuals selected at low diversity, regardless of the transplant environment. This suggests that plants at low and high diversity showed rapid evolutionary responses measurable in their phenotype. Our findings provide first empirical evidence that loss of productivity at low diversity is not only caused by changes in abiotic and biotic conditions but also that plants respond to this by a change in their micro-evolution. Thus, we conclude that eco-evolutionary feedbacks of plants at low and high diversity are critical to fully understand why the positive influence of diversity on plant productivity is strengthening through time.

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Dataset Information

Genetic drift precluded adaptation of an insect seed predator to a novel host plant in a long-term selection experiment.

Publications

Genetic drift precluded adaptation of an insect seed predator to a novel host plant in a long-term selection experiment.

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