Showing papers by "Leo W. Beukeboom published in 2021"

Artificial selection for nonreproductive host killing in a native parasitoid on the invasive pest, Drosophila suzukii

Abstract: Establishment and spread of invasive species can be facilitated by lack of natural enemies in the invaded area. Host-range evolution of natural enemies augments their ability to reduce the impact of the invader and could enhance their value for biological control. We assessed the potential of the Drosophila parasitoid, Leptopilina heterotoma (Hymenoptera: Figitidae), to exploit the invasive pest Drosophila suzukii by focusing on three performance indices: (i) attack rate; (ii) host killing, consisting of killing rate and lethal attack rate (killing efficiency); and (iii) successful offspring development (reproductive success). We found significant intraspecific variation in attack rate and killing rate and lethal attack rate among seven European populations, but offspring generally failed to successfully develop from the D. suzukii host. We crossed these European lines to create a genetically variable source population and performed a half-sib analysis to quantify genetic variation. Using a Bayesian animal model, we found that attack rate and killing rate had a heritability of h(2)=0.2, lethal attack rate h(2)=0.4, and offspring development h(2)=0. We then artificially selected wasps with the highest killing rate of D. suzukii for seven generations to test whether host-killing could be improved. There was a small and inconsistent response to selection in the three selection lines. Realized heritability (hr(2)) after four generations of selection was 0.17 but near zero after seven generations of selection. The genetic response might have been masked by an increased D. suzukii fitness resulting from adaptation to laboratory conditions. Our study reveals that native, European, L. heterotoma can attack the invasive pest, D. suzukii and significantly reduce fly survival and that different steps of the parasitization process need to be considered in the evolution of host-range. It highlights how evolutionary principles can be applied to optimize performance of native species for biological control.

A single QTL with large effect is associated with female functional virginity in an asexual parasitoid wasp

Abstract: During the transition from sexual to asexual reproduction, a suite of reproduction-related sexual traits become superfluous, and may be selected against if costly. Female functional virginity refers to asexual females resisting to mate or not fertilizing eggs after mating. These traits appear to be among the first that evolve during transitions from sexual to asexual reproduction. The genetic basis of female functional virginity remains elusive. Previously, we reported that female functional virginity segregates as expected for a single recessive locus in the asexual parasitoid wasp Asobara japonica. Here, we investigate the genetic basis of this trait by quantitative trait loci (QTL) mapping and candidate gene analyses. Consistent with the segregation of phenotypes, we found a single QTL of large effect, spanning over 4.23 Mb and comprising at least 131 protein-coding genes, of which 15 featured sex-biased expression in the related sexual species Asobara tabida. Two of the 15 sex-biased genes were previously identified to differ between related sexual and asexual population/species: CD151 antigen and nuclear pore complex protein Nup50. A third gene, hormone receptor 4, is involved in steroid hormone mediated mating behaviour. Overall, our results are consistent with a single locus, or a cluster of closely linked loci, underlying rapid evolution of female functional virginity in the transition to asexuality. Once this variant, causing rejection to mate, has swept through a population, the flanking region does not get smaller owing to lack of recombination in asexuals.

Absence of complementary sex determination in two Leptopilina species (Figitidae, Hymenoptera) and a reconsideration of its incompatibility with endosymbiont-induced thelytoky

Abstract: Complementary sex determination (CSD) is a widespread sex determination mechanism in haplodiploid Hymenoptera. Under CSD, sex is determined by the allelic state of one or multiple CSD loci. Heterozygosity at one or more loci leads to female development, whereas hemizygosity of haploid eggs and homozygosity of diploid eggs results in male development. Sexual (arrhenotokous) reproduction normally yields haploid male and diploid female offspring. Under asexual reproduction (thelytoky), diploidized unfertilized eggs develop into females. Thelytoky is often induced by bacterial endosymbionts that achieve egg diploidization by gamete duplication. As gamete duplication leads to complete homozygosity, endosymbiont-induced thelytokous reproduction is presumed to be incompatible with CSD, which relies on heterozygosity for female development. Previously, we excluded CSD in four Asobara (Braconidae) species and proposed a two-step mechanism for Wolbachia-induced thelytoky in Asobara japonica. Here, we conclusively reject CSD in two cynipid wasp species, Leptopilina heterotoma and Leptopilina clavipes. We further show that thelytoky in L. clavipes depends on Wolbachia titer but that diploidization and feminization steps cannot be separated, unlike in A. japonica. We discuss what these results reveal about the sex determination mechanism of L. clavipes and the presumed incompatibility between CSD and endosymbiont-induced thelytoky in the Hymenoptera.

Temperature-dependent effects of house fly proto-Y chromosomes on gene expression could be responsible for fitness differences that maintain polygenic sex determination.

Abstract: Sex determination, the developmental process by which sexually dimorphic phenotypes are established, evolves fast. Evolutionary turnover in a sex determination pathway may occur via selection on alleles that are genetically linked to a new master sex determining locus on a newly formed proto-sex chromosome. Species with polygenic sex determination, in which master regulatory genes are found on multiple different proto-sex chromosomes, are informative models to study the evolution of sex determination and sex chromosomes. House flies are such a model system, with male determining loci possible on all six chromosomes and a female-determiner on one of the chromosomes as well. The two most common male-determining proto-Y chromosomes form latitudinal clines on multiple continents, suggesting that temperature variation is an important selection pressure responsible for maintaining polygenic sex determination in this species. Temperature-dependent fitness effects could be manifested through temperature-dependent gene expression differences across proto-Y chromosome genotypes. These gene expression differences may be the result of cis regulatory variants that affect the expression of genes on the proto-sex chromosomes, or trans effects of the proto-Y chromosomes on genes elswhere in the genome. We used RNA-seq to identify genes whose expression depends on proto-Y chromosome genotype and temperature in adult male house flies. We found no evidence for ecologically meaningful temperature-dependent expression differences of sex determining genes between male genotypes, but we were probably not sampling an appropriate developmental time-point to identify such effects. In contrast, we identified many other genes whose expression depends on the interaction between proto-Y chromosome genotype and temperature, including genes that encode proteins involved in reproduction, metabolism, lifespan, stress response, and immunity. Notably, genes with genotype-by-temperature interactions on expression were not enriched on the proto-sex chromosomes. Moreover, there was no evidence that temperature-dependent expression is driven by chromosome-wide cis-regulatory divergence between the proto-Y and proto-X alleles. Therefore, if temperature-dependent gene expression is responsible for differences in phenotypes and fitness of proto-Y genotypes across house fly populations, these effects are driven by a small number of temperature-dependent alleles on the proto-Y chromosomes that may have trans effects on the expression of genes on other chromosomes.

A re-assessment of within-host mating behavior in the Nasonia species complex

Abstract: Insects have a wide variety of mating systems. For parasitic wasps, mating sites are often confined to where their hosts occur and this mutual interaction therefore greatly affects the evolution of alternative mating strategies. Parasitoids of the genus Nasonia (Hymenoptera: Pteromalidae) – comprising the species Nasonia vitripennis (Walker), Nasonia longicornis Darling, Nasonia giraulti Darling, and Nasonia oneida Raychouhury & Desjardins – parasitize blowfly pupae and typically mate immediately after emergence of the females from the host puparium. However, in one Nasonia species, N. giraulti, mating predominantly occurs within the host. Here, we re-assess within-host mating (WHM) rates within the Nasonia genus, using laboratory lines and field-collected hosts, including N. oneida for which no data were available yet. We confirm that WHM rates are low in N. vitripennis and N. longicornis, but high in N. giraulti. WHM is rare in N. oneida, despite its sympatry and close phylogenetic relationship with N. giraulti. Multiparasitization experiments with N. vitripennis and N. giraulti resulted in lower WHM proportions of N. giraulti. To evaluate whether this was due to an exit hole in the host pupa created by N. vitripennis males – where an exit hole may result in emergence of N. giraulti females and possibly males prior to mating – we artificially created exit holes in the host parasitized by N. giraulti only. This also yielded a lower WHM proportion. Progeny analysis of interspecific crosses of N. longicornis and N. oneida with N. giraulti, generating hybrid female but non-hybrid male offspring, revealed that WHM is largely determined by the maternal species and, hence, by the species to which the male offspring belong. We conclude that WHM is predominantly a male-mediated trait in N. giraulti, resulting from males refraining from making exit holes and mating with females inside the host. We discuss how these findings can be used to evaluate whether WHM contributes to preventing species hybridization.

Courtship rhythm in Nasonia vitripennis is affected by the clock gene period

Abstract: The clock gene period (per) is a regulator of circadian rhythms but may also play a role in the regulation of ultradian rhythms, such as insect courtship. Males of the parasitoid wasp Nasonia vitripennis court females by performing series of head movements (‘head-nods’) and wing vibrations within repeated cycles. The pattern of cycle duration and head-nod number is species-specific and has a genetic basis. In this study, the possible involvement of per in regulating Nasonia courtship rhythms was investigated in a southern and northern European strain that differ in number and timing of courtship components. Knockdown of per via RNA interference (RNAi) resulted in a shortening of the circadian free running period (tau) in constant darkness (DD), and increased both the cycle duration and the number of head-nods per cycle in both strains. These results point at a role of per in the regulation of ultradian rhythms and male courtship behaviour of N. vitripennis and may contribute to resolving the controversy about the role of per in insect courtship behaviour.

Epistatic interactions between sex chromosomes and autosomes can affect the stability of sex determination systems

Abstract: Sex determination (SD) is an essential and ancient developmental process, but the genetic systems that regulate this process are surprisingly variable. Why SD mechanisms vary so much is a longstanding question in evolutionary biology. SD genes are generally located on sex chromosomes which also carry genes that interact epistatically with autosomes to affect fitness. How this affects the evolutionary stability of SD mechanisms is still unknown. Here, we explore how epistatic interactions between a sexually antagonistic (SA) non-SD gene, located on either an ancestral or novel sex chromosome, and an autosomal gene affect the conditions under which an evolutionary transition to a new SD system occurs. We find that when the SD gene is linked to an ancestral sex chromosomal gene which engages in epistatic interactions, epistasis enhances the stability of the sex chromosomes so that they are retained under conditions where transitions would otherwise occur. This occurs both when weaker fitness effects are associated with the ancestral sex chromosome pair or stronger fitness effects associated with a newly-evolved SD gene. However, the probability that novel SD genes spread is unaffected if they arise near genes involved in epistasis. This discrepancy occurs because on autosomes, SA allele frequencies are typically lower than on sex chromosomes. In our model, increased frequencies of these alleles contribute to a higher frequency of epistasis which may therefore more readily occur on sex chromosomes. Because sex chromosome-autosome interactions are abundant and can take several forms, they may play a large role in maintaining sex chromosomes.

Entomophagous insects – an introduction

Abstract: This special issue contains papers presented at the 6th International Entomophagous Insects Conference. Entomophagous insects consume other insects. They are a fundamental component of ecosystems and are extensively used as biocontrol agents. The first article reviews the role of ladybirds in biological control and the second reviews the biological control of stink bugs. The following nine research articles cover the rearing, behavior, life history, and ecology of parasitoid and predator species.