Sex allocation theory reveals a hidden cost of neonicotinoid exposure in a parasitoid wasp

Abstract

Sex allocation theory has proved to be one the most successful theories in evolutionary ecology. However, its role in more applied aspects of ecology has been limited. Here we show how sex allocation theory helps uncover an otherwise hidden cost of neonicotinoid exposure in the parasitoid wasp Nasonia vitripennis. Female N. vitripennis allocate the sex of their offspring in line with Local Mate Competition (LMC) theory. Neonicotinoids are an economically important class of insecticides, but their deployment remains controversial, with evidence linking them to the decline of beneficial species. We demonstrate for the first time to our knowledge, that neonicotinoids disrupt the crucial reproductive behaviour of facultative sex allocation at sub-lethal, field-relevant doses in N. vitripennis. The quantitative predictions we can make from LMC theory show that females exposed to neonicotinoids are less able to allocate sex optimally and that this failure imposes a significant fitness cost. Our work highlights that understanding the ecological consequences of neonicotinoid deployment requires not just measures of mortality or even fecundity reduction among non-target species, but also measures that capture broader fitness costs, in this case offspring sex allocation. Our work also highlights new avenues for exploring how females obtain information when allocating sex under LMC.

Keywords: beneficial insects; sex ratio; systemic insecticide.

Figure 1.

Imidacloprid reduces longevity in a dose-dependent manner. The survival curve shows reduced survival for female Nasonia vitripennis fed 100 ppb or 200 ppb imidacloprid, while females fed 1 ppb or 10 ppb had survival similar to controls fed only 20% sucrose solution. Inset: a female N. vitripennis ovipositing on a blowfly host.

Figure 2.

Imidacloprid influences the reproductive output of female Nasonia vitripennis. Females were fed either 20% sucrose solution (controls) or imidacloprid at concentrations of 2 ppb, 10 ppb or 100 ppb. (a) Sex ratio (proportion male) varies with exposure to both co-foundresses and imidacloprid, with increasing dose reducing the sex ratio response to increasing co-foundress number. (b) Total offspring production is reduced by imidacloprid in a dose-independent manner. (c) Female offspring production is likewise reduced by imidacloprid across all dose levels and across all foundress numbers; the maintenance of more female-biased sex ratios regardless of foundress number when exposed to imidacloprid therefore does not lead to greater female offspring production. Error bars indicate binomial standard errors.

Figure 3.

Disruption of facultative sex allocation leads to reduced fitness when ovipositing with co-foundresses. Females were fed either 20% sucrose solution (controls) or imidacloprid at concentrations of 2 ppb, 10 ppb or 100 ppb. Fitness was calculated relative to a hypothetical female producing the evolutionary stable sex ratio.