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.

New species based on the biological species concept within the complex of Lariophagus distinguendus (Hymenoptera, Chalcidoidea, Pteromalidae), a parasitoid of household pests

“…Our results indicate that sexual isolation, albeit weak and unilateral, emerges as first barrier between closely related strains without obvious ecological separation, such as the use of different hosts, and increases in strength during the process of separation. This agrees with other data on reproductive barriers in L. distinguendus (König, Zundel, et al, 2019), and with the recent study on reproductive barriers within a population of N. vitripennis (Malec et al, 2021), where slight sexual isolation was found between closely related populations and even within a population of the same species. As in N. vitripennis, sexual isolation in L. distinguendus is most likely caused by a mate choice decision of the female, which do not accept males with diverging mandibular pheromones that are applied on the female antennae during courtship (König, Seeger, et al, 2015;Ruther & Hammerl, 2014).…”

Chemical and population genetic analysis show no evidence of ecotype formation in a European population of the parasitoid wasp Nasonia vitripennis

“…Due to the long-standing postulation of the discernibility between the bird and carrion ecotypes of N. vitripennis (Grassberger and Frank, 2004;Peters and Abraham, 2010;Malec et al, 2021), our findings that clearly do not support their unambiguous differentiation on a phenotypic and genetic level were unexpected. An important aspect largely neglected in earlier studies conducted on populations of this species is the estimation of how frequent habitat switches can occur in nature.…”

“…A recent study demonstrated very early reproductive barriers between the nest and carrion ecotypes in a sympatric N. vitripennis population from Southern Germany, hinting at premating and sexual isolation preceding ecological separation (Malec et al, 2021). Here, we focus on a sympatric N. vitripennis population from the Netherlands and test for potential degrees of separation between the different ecotypes on a phenotypic and population genetic level.…”

“…van de Zande et al, 2014;Pannebakker et al, 2020). Its most well-known and cosmopolitan species, Nasonia vitripennis, has been proposed to be differentiated into two ecotypes distinguishable by their respective microhabitats (Schröder, 2000;Malec et al, 2021; Figure 1). Females of this species parasitize a wide array of different fly pupae, most commonly from the genera Sarcophaga (flesh flies), Calliphora (blowflies) and Protocalliphora (bird blowflies).…”

The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps

“…Nicholls et al., 2010). Conversely, chalcid wasps can undergo rapid speciation by the emergence of ecotypes (Malec et al., 2021) or cytoplasmic incompatibility (Gebiola et al., 2016) and thus may be prone to sympatric speciation (König et al., 2019). Logically, the range of a parasitoid species will be limited by the range of its host(s).…”