The emergence of ecotypes in a parasitoid wasp: a case of incipient sympatric speciation in Hymenoptera?

Abstract

Background: To understand which reproductive barriers initiate speciation is a major question in evolutionary research. Despite their high species numbers and specific biology, there are only few studies on speciation in Hymenoptera. This study aims to identify very early reproductive barriers in a local, sympatric population of Nasonia vitripennis (Walker 1836), a hymenopterous parasitoid of fly pupae. We studied ecological barriers, sexual barriers, and the reduction in F1-female offspring as a postmating barrier, as well as the population structure using microsatellites.

Results: We found considerable inbreeding within female strains and a population structure with either three or five subpopulation clusters defined by microsatellites. In addition, there are two ecotypes, one parasitizing fly pupae in bird nests and the other on carrion. The nest ecotype is mainly formed from one of the microsatellite clusters, the two or four remaining microsatellite clusters form the carrion ecotype. There was slight sexual isolation and a reduction in F1-female offspring between inbreeding strains from the same microsatellite clusters and the same ecotypes. Strains from different microsatellite clusters are separated by a reduction in F1-female offspring. Ecotypes are separated only by ecological barriers.

Conclusions: This is the first demonstration of very early reproductive barriers within a sympatric population of Hymenoptera. It demonstrates that sexual and premating barriers can precede ecological separation. This indicates the complexity of ecotype formation and highlights the general need for more studies within homogenous populations for the identification of the earliest barriers in the speciation process.

Keywords: Ecological speciation; Ecotypes; Inbreeding; Postmating barrier; Premating barrier; Reproductive barriers; Sympatric speciation.

Fig. 1

Percentage of Lucilia sericata baits that had been parasitized by Nasonia vitripennis females in bird nests (yellow) and next to carrion (blue) over a sampling period of 24 weeks (end of April–mid of October 2012) in the Hohenheim Park

Fig. 2

Number of strains of Nasonia vitripennis with significant reaction to the odour of bird nests and carrion in olfactometer experiments. Wasp strains originate from bird nests (yellow) or next to carrion (blue). For each strain about 20 wasps were tested. Coloured parts of the bars refer to the number of reacting strains

Fig. 3

Number of pupae of Lucilia sericata carrion flies parasitized by Nasonia vitripennis wasps (A) and offspring emerging from these pupae (B). Wasps were collected in bird nests (yellow, n = 90) or next to carrion (blue, n = 90). The box and whisker plots show minimum, maximum, 1st and 3rd quartile, median and mean as asterisk. **: significant difference at p < 0.01 (Mann–Whitney U-test)

Fig. 4

Results from a population genetic analysis using microsatellites of a population of the parasitoid wasp Nasonia vitripennis in the park of Hohenheim, Germany, using STRUCTURE v2.3. Wasps were collected in bird nests or next to carrion. In the bar plots each individual is represented by a vertical line coloured according to its probability of assignment to one of either k = 3 (A) or k = 5 (B) subpopulations. Origin of wasps from bird nests or carrion is indicated above each graph. The affiliation of experimental strains N2, N3 N9, A1, A7, and A19 to subpopulations within the dataset is indicated below each graph

Fig. 5

Occurrence of copulation in N. vitripennis depending on origin of mating partners. A Females and males originate from the same strain (green), or from different strains but the same microsatellite cluster with k = 3 (yellow) or k = 5 (orange) subpopulations, or the same microhabitat (blue). B Females and males originate from different strains but the same microsatellite cluster with k = 3 (yellow) or k = 5 (orange), or from different microsatellite clusters (yellow/orange), or originate from the same (blue) or different microhabitats (white/blue). Coloured parts of the bar indicate the percentage of couples with copulation. Numbers in bars indicate numbers of replicates. Different letters above bars in A indicate significant differences at p < 0.01 (Tukey-test based on a generalized linear model, family “binomial”). In B, ANOVA was based on a generalized linear model, family “binomial”

Fig. 6

Influence of origin of the mating partners on number and sex ratio of F1-offspring in the parasitoid wasp Nasonia vitripennis. A F1-female offspring; B F1-male offspring; C F1-total offspring; D sex ratio. Females and males originate from the same strain (green, n = 90), or from different strains but the same microsatellite cluster with k = 3 (yellow, n = 90) or k = 5 (orange, n = 60) subpopulations, or originate from the same microhabitat (blue, n = 180). Box and whisker plots show minimum, maximum, 1st and 3rd quartile, and median. Different lower case letters indicate significant differences (p < 0.05, generalized linear models with family “quasipoisson” followed by ANOVA and Tukey-test. For test statistics see Tables 3 and 4

Fig. 7

The influence of origin of mating partners on number and sex ratio of F1-offspring in the parasitoid wasp Nasonia vitripennis. A F1-female offspring; B F1-male offspring; C F1-total offspring; D sex ratio. Mating partners originated from the same or from different microsatellite clusters (with k = 3 or k = 5 subpopulations), or from the same or different microhabitats. Box and whisker plots show minimum, maximum, 1st and 3rd quartile, and median. Levels of significance are based on generalized linear models, family “negative binomial”, followed by Tukey-test. For test statistics see Table 5

Fig. 8

Hypothetical scenarios for the emergence of the observed pattern of subpopulations and ecotypes of Nasonia vitripennis. Scenario A Inbreeding lines evolve into subpopulations in sympatry and become independently adapted to their respective microhabitats. Scenario B Inbreeding lines evolve into two subpopulations in sympatry. One subpopulation becomes adapted to bird nests as microhabitat and one subpopulation becomes adapted to carrion. Subsequently, the carrion subpopulations splits up into 2 or 4 separate subpopulations. Scenario C Subpopulations became adapted to their respective microhabitats in allopatry and become sympatric by immigration into the study area

Fig. 9

Static 4-chamber olfactometer to test the reaction of female N. vitripennis to odours of bird nest and carrion. 1: glass plate; 2: walking arena; 3: test field; 4: control field; 5: transition zone