Oviposition but Not Sex Allocation Is Associated with Transcriptomic Changes in Females of the Parasitoid Wasp Nasonia vitripennis

Abstract

Linking the evolution of the phenotype to the underlying genotype is a key aim of evolutionary genetics and is crucial to our understanding of how natural selection shapes a trait. Here, we consider the genetic basis of sex allocation behavior in the parasitoid wasp Nasonia vitripennis using a transcriptomics approach. Females allocate offspring sex in line with the local mate competition (LMC) theory. Female-biased sex ratios are produced when one or a few females lay eggs on a patch. As the number of females contributing offspring to a patch increases, less female-biased sex ratios are favored. We contrasted the transcriptomic responses of females as they oviposit under conditions known to influence sex allocation: foundress number (a social cue) and the state of the host (parasitized or not). We found that when females encounter other females on a patch or assess host quality with their ovipositors, the resulting changes in sex allocation is not associated with significant changes in whole-body gene expression. We also found that the gene expression changes produced by females as they facultatively allocate sex in response to a host cue and a social cue are very closely correlated. We expanded the list of candidate genes associated with oviposition behavior in Nasonia, some of which may be involved in fundamental processes underlying the ability to facultatively allocate sex, including sperm storage and utilization.

Exposure to the neonicotinoid imidacloprid disrupts sex allocation cue use during superparasitism in the parasitoid wasp Nasonia vitripennis

“…However, research into the mechanisms involved in sex allocation in N. vitripennis is much less advanced, both in terms of the genetic basis of sex ratio and in terms of the underlying neuroscience. Quantitative genetic studies have revealed QTL associated with sex ratio variation (Pannebakker et al, 2011), transcriptomics studies have investigated gene expression patterns associated with sex allocation (Cook et al, 2015a), and a role for epigenetics, specifically DNA methylation, has also been inferred (Cook et al, 2015b). However, we still know virtually nothing of the neural substrates of sex allocation.…”

Evidence of capacitation in the parasitoid wasp,Nasonia vitripennisand its potential role in sex allocation

“…Three studies have tried to identify gene regulatory changes in sex allocation. Cook et al 2015 and Cook et al 2018 used RNASeq and Pannebakker et al 2013 used a microarray approach, to try and identify key genes that could be involved in sex allocation. The 2015 study used whole bodies and compared three conditions; no host, fresh host and parasitised host to investigate the difference in oviposition and how increased female biased broods in the fresh host compared to the previoously parasitised host.…”

“…No differentially expressed genes were identified, indicating that if there are changes in gene expression involved in sex allocation they don’t occur in the brain. The expression of the sex determining splicing factor double sex ( dsx ) was altered in relation to oviposition (Cook et al , 2015). Female and male specific splice variants need to be maternally provided for normal sex determination pathways to work (Verhulst et al , 2010, 2013).…”

“…In the eusocial Hymenoptera, alternative splicing has an important role in reproductive status (Price et al , 2018; Jarosch et al , 2011). We also see alternative splicing involved in neurotransmitter receptors within Hymenoptera (Jin et al , 2007) which have been linked to oviposition in N. vitripennis and the regulation of sex allocation by neuronal signalling (Cook et al , 2015). In fact, application of the neurotransmitter acetylcholine agonist imidicloprid to N vitripennis , disrupts the detection of the optimal sex allocation (Cook et al , 2016).…”

“…We used the 2015 data from Cook et al 2015 and the 2018 data from Cook et al 2018 to investigate alternative splicing and sex allocation. Our aim is to identify if alternative splicing could be involved directly in sex allocation, by searching for an effect caused by foundress number.…”