Evolution of sex-specific wing shape at the widerwing locus in four species of Nasonia

Abstract

How do morphological differences between species evolve at the genetic level? This study investigates the genetic basis of recent divergence in male wing size between species of the model parasitoid wasp Nasonia. The forewings of flightless Nasonia vitripennis males are 2.3 times smaller than males of their flighted sister species N. giraulti. We describe a major genetic contributor to this difference: the sex-specific widerwing (wdw) locus, which we have backcrossed from N. giraulti into N. vitripennis and mapped to an 0.9 megabase region of chromosome 1. This introgression of wdw from large-winged N. giraulti into small-winged N. vitripennis increases male but not female forewing width by 30% through wing region-specific size changes. Indirect evidence suggests that cell number changes across the wing explain the majority of the wdw wing-size difference, whereas changes in cell size are important in the center of the wing. Introgressing the same locus from the other species in the genus, N. longicornis and N. oneida, into N. vitripennis produces intermediate and large male wing sizes. To our knowledge, this is the first study to introgress a morphological quantitative trait locus (QTL) from multiple species into a common genetic background. Epistatic interactions between wdw and other QTL are also identified by introgressing wdw from N. vitripennis into N. giraulti. The main findings are (1) the changes at wdw have sex- and region-specific effects and could, therefore, be regulatory, (2) the wdw locus seems to be a co-regulator of cell size and cell number, and (3) the wdw locus has evolved different wing width effects in three species.

Fig. 1

Male forewing size differs across the Nasonia genus and in introgressions of the wdw locus from each species, but female forewings of wdw introgressions are not affected. Cladogram depicts relationships between the Nasonia species (Raychoudhury et al. 2009). Scale bar: 200um.

Fig. 2

Landmarks, axes and wing regions used in this study. Black lines represent the length (P-D) and width (A-P) axes. Arrowheads show forewing landmarks used for calculating distances along the A-P axis. Regions used for seta counts are depicted with numbers and are defined by landmarks (white circles) placed at the intersection of either the wing margin, folds (thick white curves) or translations of the A-P and P-D axis (thin white lines).

Fig. 3

Map of the wdw region. Genotype at length polymorphism (indel) markers is shown for the three wdw_gV introgressions. Dotted line: Consensus location of the wdw QTL based on shared overlapping markers in the region. Black bars: N. vitripennis (background) genotype. Open bars: N. giraulti (introgression) genotype. Shading: Genotype between two markers is unknown. Marker locations in SCAFFOLD1 and map data for other introgressions are given in Appendix 1.

Fig. 4

Seta number, area and shape contributions to forewing regions. a: Change averaged across all twelve seta-containing regions. b: The largest changed region (region 6) shows local area-per-seta effects. Interseta shape values greater than one indicate that seta are farther apart along the A-P (width) axis. Relative mean ± standard deviation is shown. Letters denote contrast groups for multiple comparisons (Tukey’s HSD, n=b=8).

Fig. 5

Compositional epistasis between wdw and genetic background. If wdw does not interact with other QTL in the species background and wing length (for example) is additive, Δlength[V] should equal Δlength[G].