The effects of agent hybridization on the efficacy of biological control of tansy ragwort at high elevations

Abstract The success rate of weed biological control programs is difficult to evaluate and the factors affecting it remain poorly understood. One aspect which is still unclear is whether releases of multiple, genetically distinct populations of a biological control agent increase the likelihood of s...

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Main Authors: Marianna Szűcs, Patricia E. Salerno, Brittany J. Teller, Urs Schaffner, Jeffrey L. Littlefield, Ruth A. Hufbauer
Format: Article
Language:English
Published: Wiley 2019-03-01
Series:Evolutionary Applications
Subjects:
Online Access:https://doi.org/10.1111/eva.12726
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author Marianna Szűcs
Patricia E. Salerno
Brittany J. Teller
Urs Schaffner
Jeffrey L. Littlefield
Ruth A. Hufbauer
author_facet Marianna Szűcs
Patricia E. Salerno
Brittany J. Teller
Urs Schaffner
Jeffrey L. Littlefield
Ruth A. Hufbauer
author_sort Marianna Szűcs
collection DOAJ
description Abstract The success rate of weed biological control programs is difficult to evaluate and the factors affecting it remain poorly understood. One aspect which is still unclear is whether releases of multiple, genetically distinct populations of a biological control agent increase the likelihood of success, either by independent colonization of different environmental niches or by hybridization that may increase the agent's fitness and adaptive ability. Since hybridization is often invoked to explain the success of unintentionally introduced exotic species, hybridization among biocontrol agents may be similarly important in shaping the effectiveness of biological control programs. In this study, we first evaluated intraspecific hybridization among populations of a weed biological control agent, the ragwort flea beetle, Longitarsus jacobaeae. These insects were introduced as part of a classical biological control program from Italy and Switzerland. We genotyped 204 individuals from 15 field sites collected in northwest Montana, and an additional 52 individuals that served as references for Italian and Swiss populations. Bayesian analysis of population structure assigned seven populations as pure Swiss and one population as pure Italian, while intraspecific hybrid individuals were detected in seven populations at frequencies of 5%–69%. Subsequently, we conducted a 2‐year exclusion experiment using six sites with Swiss beetles and three with hybrid beetles to evaluate the impact of biological control. We found that biological control by Swiss beetles and by hybrid beetles is effective, increasing mortality of the target plant, Jacobaea vulgaris, by 42% and 45%, and reducing fecundity of surviving plants by 44% and 72%, respectively. Beetle densities were higher and mortality of larger plants was higher at sites with hybrids present. These results suggest that hybridization of ragwort flea beetles at high‐elevation sites may improve biological control of tansy ragwort and that intraspecific hybridization of agents could benefit biological control programs.
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spelling doaj.art-3135c7b597b94228b6a69fd02cb65f5d2022-12-22T01:10:52ZengWileyEvolutionary Applications1752-45712019-03-0112347048110.1111/eva.12726The effects of agent hybridization on the efficacy of biological control of tansy ragwort at high elevationsMarianna Szűcs0Patricia E. Salerno1Brittany J. Teller2Urs Schaffner3Jeffrey L. Littlefield4Ruth A. Hufbauer5Department of Entomology Michigan State University East Lansing MichiganDepartment of Biology Colorado State University Fort Collins ColoradoDepartment of Biology Pennsylvania State University State College PennsylvaniaCentre for Agriculture and Biosciences International Delémont SwitzerlandDepartment of Land Resources and Environmental Sciences Montana State University Bozeman MontanaDepartment of Bioagricultural Sciences and Pest Management Colorado State University Fort Collins ColoradoAbstract The success rate of weed biological control programs is difficult to evaluate and the factors affecting it remain poorly understood. One aspect which is still unclear is whether releases of multiple, genetically distinct populations of a biological control agent increase the likelihood of success, either by independent colonization of different environmental niches or by hybridization that may increase the agent's fitness and adaptive ability. Since hybridization is often invoked to explain the success of unintentionally introduced exotic species, hybridization among biocontrol agents may be similarly important in shaping the effectiveness of biological control programs. In this study, we first evaluated intraspecific hybridization among populations of a weed biological control agent, the ragwort flea beetle, Longitarsus jacobaeae. These insects were introduced as part of a classical biological control program from Italy and Switzerland. We genotyped 204 individuals from 15 field sites collected in northwest Montana, and an additional 52 individuals that served as references for Italian and Swiss populations. Bayesian analysis of population structure assigned seven populations as pure Swiss and one population as pure Italian, while intraspecific hybrid individuals were detected in seven populations at frequencies of 5%–69%. Subsequently, we conducted a 2‐year exclusion experiment using six sites with Swiss beetles and three with hybrid beetles to evaluate the impact of biological control. We found that biological control by Swiss beetles and by hybrid beetles is effective, increasing mortality of the target plant, Jacobaea vulgaris, by 42% and 45%, and reducing fecundity of surviving plants by 44% and 72%, respectively. Beetle densities were higher and mortality of larger plants was higher at sites with hybrids present. These results suggest that hybridization of ragwort flea beetles at high‐elevation sites may improve biological control of tansy ragwort and that intraspecific hybridization of agents could benefit biological control programs.https://doi.org/10.1111/eva.12726classical weed biological controlddRADheterosisintraspecific hybridization
spellingShingle Marianna Szűcs
Patricia E. Salerno
Brittany J. Teller
Urs Schaffner
Jeffrey L. Littlefield
Ruth A. Hufbauer
The effects of agent hybridization on the efficacy of biological control of tansy ragwort at high elevations
Evolutionary Applications
classical weed biological control
ddRAD
heterosis
intraspecific hybridization
title The effects of agent hybridization on the efficacy of biological control of tansy ragwort at high elevations
title_full The effects of agent hybridization on the efficacy of biological control of tansy ragwort at high elevations
title_fullStr The effects of agent hybridization on the efficacy of biological control of tansy ragwort at high elevations
title_full_unstemmed The effects of agent hybridization on the efficacy of biological control of tansy ragwort at high elevations
title_short The effects of agent hybridization on the efficacy of biological control of tansy ragwort at high elevations
title_sort effects of agent hybridization on the efficacy of biological control of tansy ragwort at high elevations
topic classical weed biological control
ddRAD
heterosis
intraspecific hybridization
url https://doi.org/10.1111/eva.12726
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