The genetic basis of interspecies host preference differences in the model parasitoid Nasonia

Abstract

The genetic basis of host preference has been investigated in only a few species. It is relevant to important questions in evolutionary biology, including sympatric speciation, generalist versus specialist adaptation, and parasite-host co-evolution. Here we show that a major locus strongly influences host preference in Nasonia. Nasonia are parasitic wasps that utilize fly pupae; Nasonia vitripennis is a generalist that parasitizes a diverse set of hosts, whereas Nasonia giraulti specializes in Protocalliphora (bird blowflies). In laboratory choice experiments using Protocalliphora and Sarcophaga (flesh flies), N. vitripennis shows a preference for Sarcophaga, whereas N. giraulti shows a preference for Protocalliphora. Through a series of interspecies crosses, we have introgressed a major locus affecting host preference from N. giraulti into N. vitripennis. The N. giraulti allele is dominant and greatly increases preference for Protocalliphora pupae in the introgression line relative to the recessive N. vitripennis allele. Through the utilization of a Nasonia genotyping microarray, we have identified the introgressed region as 16 Mb of chromosome 4, although a more complete analysis is necessary to determine the exact genetic architecture of host preference in the genus. To our knowledge, this is the first introgression of the host preference of one parasitoid species into another, as well as one of the few cases of introgression of a behavioral gene between species.

Figure 1

Generation of the bkbw_g introgression line and map of visible markers in the region. In the parental cross, N. giraulti females were mated to N. vitripennis peach males. In each backcross generation, heterozygous females, identified by visible markers (m) in the bkbw_g region, were mated to N. vitripennis peach males to further reduce the size of the introgression. To purebreed the line, heterozygous bkbw_g/+_v females were mated to bkbw_g introgression males, and their homozygous bkbw_g/ bkbw_g introgression female offspring were again mated to bkbw_g introgression males in an attempt to produce an isogenic line. Inset is a map of the bkbw_g region, including the location of visible markers ws1 (wing size 1), bl13 (blue 13), bk576 (black 576), and sww (shorter wider wings). Markers indicated with asterisks were used to track the bkbw_g introgression. Distances between visible markers are shown in centiMorgans (cM).

Figure 2

Behavior of wasps in host preference experiments. N. vitripennis strains ASymCx and peach, N. giraulti strain RV2Xu, and heterozygous bkbw_g/+_v introgression females were tested. Genetic content of the wasps is shown in the chromosomes to the right, with white representing N. vitripennis DNA and black representing N. giraulti DNA. As can be seen, heterozygous bkbw_g/+_v females contain a small region of N. giraulti DNA in a largely N. vitripennis genetic background. Wasps were given one Sarcophaga and one Protocalliphora host and observed for 4.5 hours. The percent which contacted and stung each host is shown, and error bars indicate standard error of proportions (Sokal and Rohlf, 1969). Sample size for each strain is given to the right of the strain names.

Figure 3

Time spent on hosts by wasps in host acceptance and preference experiments. N. vitripennis strains ASymCx and peach, N. giraulti strain RV2Xu, and heterozygous bkbw_g/+_v introgression females were tested. Percent time is based on 28 observations over a 4.5 hour period. Sample sizes for each strain in each experiment are shown to the right of the strain names. The relative sizes of Sarcophaga and Protocalliphora hosts are also shown.