Abstract

Climate change can increase spatial synchrony of population dynamics, leading to large-scale fluctuation that destabilizes communities. High trophic level species such as parasitoids are disproportionally affected because they depend on unstable resources. Most parasitoid wasps have complementary sex determination, producing sterile males when inbred, which can theoretically lead to population extinction via the diploid male vortex (DMV). We examined this process empirically using a hyperparasitoid population inhabiting a spatially structured host population in a large fragmented landscape. Over four years of high host butterfly metapopulation fluctuation, diploid male production by the wasp increased, and effective population size declined precipitously. Our multitrophic spatially structured model shows that host population fluctuation can cause local extinctions of the hyperparasitoid because of the DMV. However, regionally it persists because spatial structure allows for efficient local genetic rescue via balancing selection for rare alleles carried by immigrants. This is, to our knowledge, the first empirically based study of the possibility of the DMV in a natural host–parasitoid system.

Highlights

  • The frequency of weather extremes is increasing under ongoing climate change [1]

  • We present a scenario in which large fluctuations in population dynamics of a herbivore due to environmental change propagate up through the food chain, affecting a 4th-trophic-level hyperparasitoid, both demographically and genetically

  • We show the importance of spatial population structure and genetic rescue among local

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Summary

Introduction

The frequency of weather extremes is increasing under ongoing climate change [1]. One repercussion of extreme events is increased spatial synchrony of local populations [2], which can decrease stability regionally and alter biotic interactions and community structure [3]. Our study demonstrates the long-term impact of increased fluctuations in the population dynamics of the host butterfly (the second trophic level) on the population size of a hyperparasitoid (the fourth trophic level), mediated through both demographic processes and loss of genetic diversity at the CSD locus. We developed a discrete-time individual-based simulation model of spatially structured populations of a hyperparasitoid including explicit genetics for CSD. It simulates the population dynamics of the hyperparasitoid in response to fluctuation and spatial autocorrelation of local butterfly populations. We modelled the mean rate of hyperparasitism at time t in sub-region i, fi,t, as a saturating function of the ratio between hyperparasitoid female and parasitoid densities, and visually fit the function to empirical data (electronic supplementary material, E1 and figure S2). B 285: 20180372 migration rate small sub-region size medium low

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