Genomics of sex allocation in the parasitoid wasp Nasonia vitripennis

Abstract

Background: Whilst adaptive facultative sex allocation has been widely studied at the phenotypic level across a broad range of organisms, we still know remarkably little about its genetic architecture. Here, we explore the genome-wide basis of sex ratio variation in the parasitoid wasp Nasonia vitripennis, perhaps the best studied organism in terms of sex allocation, and well known for its response to local mate competition.

Results: We performed a genome-wide association study (GWAS) for single foundress sex ratios using iso-female lines derived from the recently developed outbred N. vitripennis laboratory strain HVRx. The iso-female lines capture a sample of the genetic variation in HVRx and we present them as the first iteration of the Nasonia vitripennis Genome Reference Panel (NVGRP 1.0). This panel provides an assessment of the standing genetic variation for sex ratio in the study population. Using the NVGRP, we discovered a cluster of 18 linked SNPs, encompassing 9 annotated loci associated with sex ratio variation. Furthermore, we found evidence that sex ratio has a shared genetic basis with clutch size on three different chromosomes.

Conclusions: Our approach provides a thorough description of the quantitative genetic basis of sex ratio variation in Nasonia at the genome level and reveals a number of inter-related candidate loci underlying sex allocation regulation.

Keywords: Genetic reference panel; Genome-wide association study (GWAS); Local mate competition; Nasonia; Oviposition; Parasitoid wasp; Sex allocation; Single nucleotide polymorphism (SNP).

Fig. 1

Mean nucleotide diversity π (upper panel), mean number of segregating sites Watterson’s θ (middle panel) and Tajima’s D (lower panel) over non-overlapping 400 kb windows across the chromosomes in NVGRP (red and blue lines) and the HVRx laboratory outbred population (grey and black lines)

Fig. 2

Decay of linkage disequilibrium with physical distance. Dots shows the r² among pairs of SNPs, red solid line gives the non-linear least squares fit of r² on the distance between pairs of SNP. Dashed line indicates the half-decay LD distance at 17.8 kb

Fig. 3

Linkage disequilibrium half-decay distance across the genome. For each SNP on each of the five chromosomes, the log₁₀(LD half-decay distance) is plotted

Fig. 4

Manhattan plot for offspring sex ratio (top panel) and brood size (bottom panel) in N. vitripennis in the GWAS experiment, showing –log10(P)-values of the single marker regressions for every polymorphic SNP across the chromosomes of the Nasonia vitripennis Genetic Reference Panel (NVGRP). Red line indicates the empirical threshold at a q-value of 0.1, corresponding to P = 2.00*10–6, or –log10(P) = 5.70 for sex ratio. Green highlighted SNPs show the 400 kb windows in which the P-values for sex ratio and brood size overlap more than expected by chance