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Temperature-driven range expansion of an irruptive insect heightened by weakly coevolved plant defenses.

ABSTRACT: Warming climate has increased access of native bark beetles to high-elevation pines that historically received only intermittent exposure to these tree-killing herbivores. Here we show that a dominant, relatively naïve, high-elevation species, whitebark pine, has inferior defenses against mountain pine beetle compared with its historical lower-elevation host, lodgepole pine. Lodgepole pines respond by exuding more resin and accumulating higher concentrations of toxic monoterpenes than whitebark pine, where they co-occur. Furthermore, the chemical composition of whitebark pine appears less able to inhibit the pheromonal communication beetles use to jointly overcome tree defenses. Despite whitebark pine's inferior defenses, beetles were more likely to attack their historical host in mixed stands. This finding suggests there has been insufficient sustained contact for beetles to alter their complex behavioral mechanisms driving host preference. In no-choice assays, however, beetles readily entered and tunneled in both hosts equally, and in stands containing less lodgepole pine, attacks on whitebark pines increased. High-elevation trees in pure stands may thus be particularly vulnerable to temperature-driven range expansions. Predators and competitors were more attracted to volatiles from herbivores attacking their historical host, further increasing risk in less coevolved systems. Our results suggest cold temperatures provided a sufficient barrier against herbivores for high-elevation trees to allocate resources to other physiological processes besides defense. Changing climate may reduce the viability of that evolutionary strategy, and the life histories of high-elevation trees seem unlikely to foster rapid counter adaptation. Consequences extend from reduced food supplies for endangered grizzly bears to altered landscape and hydrological processes.

SUBMITTER: Raffa KF

PROVIDER: S-EPMC3568305 | biostudies-literature | 2013 Feb

REPOSITORIES: biostudies-literature

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Temperature-driven range expansion of an irruptive insect heightened by weakly coevolved plant defenses.

Raffa Kenneth F KF Powell Erinn N EN Townsend Philip A PA

Proceedings of the National Academy of Sciences of the United States of America 20121231 6

Warming climate has increased access of native bark beetles to high-elevation pines that historically received only intermittent exposure to these tree-killing herbivores. Here we show that a dominant, relatively naïve, high-elevation species, whitebark pine, has inferior defenses against mountain pine beetle compared with its historical lower-elevation host, lodgepole pine. Lodgepole pines respond by exuding more resin and accumulating higher concentrations of toxic monoterpenes than whitebark ...[more]

PMID: 23277541

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Project description:BackgroundEvolutionary processes can cause strong spatial genetic signatures, such as local loss of genetic diversity, or conflicting histories from mitochondrial versus nuclear markers. Investigating these genetic patterns is important, as they may reveal obscured processes and players. The maternally inherited bacterium Wolbachia is among the most widespread symbionts in insects. Wolbachia typically spreads within host species by conferring direct fitness benefits, and/or by manipulating its host reproduction to favour infected over uninfected females. Under sufficient selective advantage, the mitochondrial haplotype associated with the favoured maternally-inherited symbiotic strains will spread (i.e. hitchhike), resulting in low mitochondrial genetic variation across the host species range.MethodThe common bluetail damselfly (Ischnura elegans: van der Linden, 1820) has recently emerged as a model organism for genetics and genomic signatures of range expansion during climate change. Although there is accumulating data on the consequences of such expansion on the genetics of I. elegans, no study has screened for Wolbachia in the damselfly genus Ischnura. Here, we present the biogeographic variation in Wolbachia prevalence and penetrance across Europe and Japan (including samples from 17 populations), and from close relatives in the Mediterranean area (i.e. I. genei: Rambur, 1842; and I. saharensis: Aguesse, 1958).ResultsOur data reveal (a) multiple Wolbachia-strains, (b) potential transfer of the symbiont through hybridization, (c) higher infection rates at higher latitudes, and (d) reduced mitochondrial diversity in the north-west populations, indicative of hitchhiking associated with the selective sweep of the most common strain. We found low mitochondrial haplotype diversity in the Wolbachia-infected north-western European populations (Sweden, Scotland, the Netherlands, Belgium, France and Italy) of I. elegans, and, conversely, higher mitochondrial diversity in populations with low penetrance of Wolbachia (Ukraine, Greece, Montenegro and Cyprus). The timing of the selective sweep associated with infected lineages was estimated between 20,000 and 44,000 years before present, which is consistent with the end of the last glacial period about 20,000 years.ConclusionsOur findings provide an example of how endosymbiont infections can shape spatial variation in their host evolutionary genetics during postglacial expansion. These results also challenge population genetic studies that do not consider the prevalence of symbionts in many insects, which we show can impact geographic patterns of mitochondrial genetic diversity.

Dataset Information

Temperature-driven range expansion of an irruptive insect heightened by weakly coevolved plant defenses.

Publications

Temperature-driven range expansion of an irruptive insect heightened by weakly coevolved plant defenses.

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