Increased fluctuation in a butterfly metapopulation leads to diploid males and decline of a hyperparasitoid

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.

The effects of functional response and host abundance fluctuations on genetic rescue in parasitoids with single‐locus sex determination

“…These values follow empirically observed ranges in a previously studied system (Nair et al, 2018). Temporally autocorrelated host abundance is generated by assuming a multiplicative effect of the noise…”

“…Modified from figure 3a in Zayed and Packer (2005) Adverse external factors (e.g., habitat loss, fragementation, pesticide application, climage change) boost parasitoid persistence. Two other studies examined particular systems with empirically parameterized models and likewise reported resilience of parasitoid populations (Nair et al, 2018;Weis et al, 2017). Nair et al (2018) reported that, although the proportion of DMs increased by threefold in the population of a parasitoid after the host populations crashed, their modeling results indicated little imminent risk of a diploid male vortex even if the host fluctuates with similar variability.…”

“…Empirical evidence of the diploid male vortex in literature is, however, limited, and existing studies provide suggestive but inconclusive evidence (de Boer et al, 2015;Boff et al, 2014;Nair et al, 2018;Soro et al, 2016;Takahashi et al, 2008;Zayed & Packer, 2001).…”

“…The fragility of populations with sl-CSD suggested by Zayed and Packer (2005) seems also counter to the facts that over 80 species of hymenopterans with known sl-CSD exist in nature (Harpur et al, 2012;Heimpel & de Boer, 2008;van Wilgenburg et al, 2006) and that hymenopterans are one of the most specious taxa (Gaston, 1991;Godfray, 1994). Previous modeling studies have shown that a diploid male vortex may not occur as readily in nature because migration and negative frequency-dependent selection can maintain allelic variation at the CSD loci in spatially structured populations (Hein et al, 2009;Nair et al, 2018) and because coupled dynamics of host and parasitoid populations dampen unstable oscillations (Bompard et al, 2016). Hein et al (2009) found that, using a general competition model, initiation of a diploid male vortex would require stringent life history traits (e.g., low fertility of DMs, almost no dispersal), as seemingly small changes in these traits could F I G U R E 1 (a) A schematic diagram of the inheritance of the single-locus complementary sex determination (sl-CSD) system.…”

“…Hein et al (2009) found that, using a general competition model, initiation of a diploid male vortex would require stringent life history traits (e.g., low fertility of DMs, almost no dispersal), as seemingly small changes in these traits could F I G U R E 1 (a) A schematic diagram of the inheritance of the single-locus complementary sex determination (sl-CSD) system. Modified from figure 1 in Nair et al (2018). (b) External factors can drive populations to become small, which could trigger the negative feedback between small population size and diploid male production (due to increased inbreeding), potentially leading to extinction in an extinction vortex.…”