Influence of microbe-associated parthenogenesis on the fecundity ofTrichogramma deion andT. pretiosum

Microbe-associated parthenogenesis (thelytoky) has been discovered in nineTrichogramma species, parasitoids of mainly lepidopteran eggs. Parthenogenetic and bisexual conspecifics co-occur in many field populations. As an initial step to understand the dynamics of these two reproductive strategies we studied the effect of microbe-associated parthenogenesis on fecundity. The fecundity of two parthenogenetic isofemale lines ofT. pretiosum and one ofT. deion was compared with bisexual lines derived from them by antibiotic treatment. In all three cases parthenogenetic females were less fecund over their lifetime than bisexual females. Also, parthenogenetic females produced fewer daughters in two cases and in one case a similar number of daughters as their respective bisexual counterparts. The lack of mating and insemination was excluded as an explanation for the reduced fecundity of parthenogenetic females, because mated and virgin parthenogenetic females produce the same number of offspring. Antibiotic treatment can also be excluded because females of field-collected bisexual line treated with antibiotics produced the same number of offspring as untreated females. The reduced fecundity of parthenogenetic females was caused by a lower number of eggs being laid rather than by a greater developmental mortality. Parthenogenetic females produced less daughters than bisexual females when host availability was not limiting, but when host availability was severely limited, parthenogenetic females produced more daughters than the bisexual females.     

Parthenogenesis in Hexapoda: holometabolous insects

This study is a second part of a review on parthenogenesis in Hexapoda. In contrast to the first part describing parthenogenetic groups of Entognatha and non‐holometabolous insects (Journal of Zoological Systematics and Evolutionary Research, 54, 2016, 257), this study deals with parthenogenesis in Holometabola. For each order of this group, the main parthenogenetic taxa and modes of parthenogenesis are listed. Data on parthenogenesis across Holometabola as well as other insects are summarized and discussed.     

Maintenance and loss of heterozygosity in a thelytokous lineage of honey bees (Apis mellifera capensis)

An asexual lineage that reproduces by automictic thelytokous parthenogenesis has a problem: rapid loss of heterozygosity resulting in effective inbreeding. Thus, the circumstances under which rare asexual lineages thrive provide insights into the trade-offs that shape the evolution of alternative reproductive strategies across taxa. A socially parasitic lineage of the Cape honey bee, Apis mellifera capensis, provides an example of a thelytokous lineage that has endured for over two decades. It has been proposed that cytological adaptations slow the loss of heterozygosity in this lineage. However, we show that heterozygosity at the complementary sex determining (csd) locus is maintained via selection against homozygous diploid males that arise from recombination. Further, because zygosity is correlated across the genome, it appears that selection against diploid males reduces loss of homozygosity at other loci. Selection against homozygotes at csd results in substantial genetic load, so that if a thelytokous lineage is to endure, unusual ecological circumstances must exist in which asexuality permits such a high degree of fecundity that the genetic load can be tolerated. Without these ecological circumstances, sex will triumph over asexuality. In A. m. capensis, these conditions are provided by the parasitic interaction with its conspecific host, Apis mellifera scutellata.     

The incidence and diversity of Wolbachia in gallwasps (Hymenoptera; Cynipidae) on oak

Wolbachia bacteria infect approximately 20% of all insect species, and cause a range of alterations to host reproduction, including imposition of thelytoky. The incidence and phenotypic impact of Wolbachia remains to be established in many insect taxa, and considerable research effort is currently focused on its association with particular reproductive modes and the relative importance of the various pathways via which infection occurs. Gallwasps represent an attractive system for addressing these issues for two reasons. First, they show a diversity of reproductive modes (including arrhenotoky, thelytoky and cyclical parthenogenesis) in which the impact of Wolbachia infection can be examined. Second, they occupy two intimately linked trophic niches (gall-inducers and inquilines) between which there is potential for the horizontal exchange of Wolbachia infection. In the arrhenotokous gallwasp lineages screened to date (the herb-galling 'Aylacini' and the rose-galling Diplolepidini), Wolbachia infection always induces thelytoky. The impact of Wolbachia in other arrhenotokous clades, and in the cyclically parthenogenetic clades remains unknown. Here we use polymerase chain reaction (PCR) screening and sequence data for two Wolbachia genes (wsp and ftsZ) to examine the prevalence and incidence of Wolbachia infection in 64 species (a total of 609 individuals) in two further tribes: the arrhenotokous inquilines (tribe Synergini), and the cyclically parthenogenetic oak gallwasps (tribe Cynipini). We ask: (i) whether Wolbachia infection has any apparent impact on host reproduction in the two tribes and (ii) whether there is any correlation between Wolbachia infection and the apparent lack of an arrhenotokous generation in many oak gallwasp life cycles. We show: (i) that Wolbachia infection is rare in the Cynipini. Infected species show no deviation from cyclical parthenogenesis, and infection is no more common in species known only from a thelytokous generation; (ii) that there is a higher incidence of infection within the arrhenotokous inquilines, and generally in gallwasp tribes without cyclical parthenogensis; (iii) all Wolbachia-positive inquiline species are known to possess males, implying either that Wolbachia infection does not result in loss of sex in this tribe or, more probably, that (as for some rose gallwasps) Wolbachia infection leads to loss of sex in specific populations; and (iv) although we find some inquilines and gall inducers to be infected with Wolbachia having the same wsp sequence, these hosts are not members of the same gall communities, arguing against frequent horizontal transmission between these two trophic groups. We suggest that exchange may be mediated by the generalist parasitoids common in oak galls.     

Cape honeybees, Apis mellifera capensis, police worker-laid eggs despite the absence of relatedness benefits

In the Cape honeybee, Apis mellifera capensis, workers lay diploid(female) eggs via thelytoky. In other A. mellifera subspecies,workers lay haploid (male) eggs via arrhenotoky. When thelytokousworker reproduction occurs, worker policing has no relatednessbenefit because workers are equally related to their sisterworkers' clonal offspring and their mother queen's female offspring.We studied worker policing in A. m. capensis and in the arrhenotokousAfrican honeybee A. m. scutellata by quantifying the removalrates of worker-laid and queen-laid eggs. Discriminator coloniesof both subspecies policed worker-laid eggs of both their ownand the other subspecies. The occurrence of worker policing,despite the lack of relatedness benefit, in A. m. capensis stronglysuggests that worker reproduction is costly to the colony andthat policing is maintained because it enhances colony efficiency.In addition, because both subspecies policed each others eggs,it is probable that the mechanism used in thelytokous A. m.capensis to discriminate between queen-laid and worker-laideggs is the same as in arrhenotokous A. m. scutellata.     

Patterns and mechanisms in instances of endosymbiont‐induced parthenogenesis

Female‐producing parthenogenesis can be induced by endosymbionts that increase their transmission by manipulating host reproduction. Our literature survey indicates that such endosymbiont‐induced parthenogenesis is known or suspected in 124 host species from seven different arthropod taxa, with Wolbachia as the most frequent endosymbiont (in 56–75% of host species). Most host species (81%, 100 out of 124) are characterized by haplo‐diploid sex determination, but a strong ascertainment bias likely underestimates the frequency of endosymbiont‐induced parthenogenesis in hosts with other sex determination systems. In at least one taxon, hymenopterans, endosymbionts are a significant driver of transitions from sexual to parthenogenetic reproduction, with one‐third of lineages being parthenogenetic as a consequence of endosymbiont infection. Endosymbiont‐induced parthenogenesis appears to facilitate the maintenance of reproductive polymorphism: at least 50% of species comprise both sexual (uninfected) and parthenogenetic (infected) strains. These strains feature distribution differences similar to the ones documented for lineages with genetically determined parthenogenesis, with endosymbiont‐induced parthenogens occurring at higher latitudes than their sexual relatives. Finally, although gamete duplication is often considered as the main mechanism for endosymbiont‐induced parthenogenesis, it underlies parthenogenesis in only half of the host species studied thus far. We point out caveats in the methods used to test for endosymbiont‐induced parthenogenesis and suggest specific approaches that allow for firm conclusions about the involvement of endosymbionts in the origin of parthenogenesis.     

Manipulation of oviposition choice of the parasitoid wasp, Encarsia pergandiella, by the endosymbiotic bacterium Cardinium

Reproductive manipulations of hosts by maternally inherited bacterial endosymbionts often result in an increase in the proportion of infected female hosts in the population. When this involves the conversion of incipient males to genetic or functional females, it presents unique difficulties for symbionts invading hosts with sex-specific reproductive behaviours, such as the autoparasitic Encarsia pergandiella. In sexual forms of this species, female eggs are laid in whitefly nymphs and male eggs are laid in conspecific or heterospecific parasitoids developing within the whitefly cuticle. Further, eggs laid in the 'wrong' host do not ordinarily complete development. This study explored the role of a bacterial symbiont, Cardinium, in manipulating oviposition behaviour in a thelytokous population of E. pergandiella. Oviposition choice was measured by the number and location of eggs deposited by both infected and uninfected adult waSPS in arenas containing equal numbers of hosts suitable for the development of male and female waSPS. Uninfected waSPS included antibiotic-treated female waSPS and (untreated) daughters of antibiotic-treated female waSPS. The choices of waSPS in the thelytokous population treatments were compared with those of a conspecific sexual population. We found that offspring of antibiotic-cured thelytokous waSPS reverted to the behaviour of unmated sexual waSPS, laying their few eggs almost exclusively in hosts appropriate for male eggs. Infected thelytokous waSPS distributed their eggs approximately evenly between host types, much like mated sexual female waSPS. The antibiotic-treated female waSPS exhibited choices intermediate to waSPS in the other two treatments. The change in the observed behaviour appears sufficient to allow invasion and persistence of Cardinium in sexual populations. Lastly, our results suggest a reduction in host discrimination as a possible mechanism by which Cardinium influences this change.     

Epidemiology of asexuality induced by the endosymbiotic Wolbachia across phytophagous wasp species: host plant specialization matters

Among eukaryotes, sexual reproduction is by far the most predominant mode of reproduction. However, some systems maintaining sexuality appear particularly labile and raise intriguing questions on the evolutionary routes to asexuality. Thelytokous parthenogenesis is a form of spontaneous loss of sexuality leading to strong distortion of sex ratio towards females and resulting from mutation, hybridization or infection by bacterial endosymbionts. We investigated whether ecological specialization is a likely mechanism of spread of thelytoky within insect communities. Focusing on the highly specialized genus Megastigmus (Hymenoptera: Torymidae), we first performed a large literature survey to examine the distribution of thelytoky in these wasps across their respective obligate host plant families. Second, we tested for thelytoky caused by endosymbionts by screening in 15 arrhenotokous and 10 thelytokous species for Wolbachia, Cardinium, Arsenophonus and Rickettsia endosymbionts and by performing antibiotic treatments. Finally, we performed phylogenetic reconstructions using multilocus sequence typing (MLST) to examine the evolution of endosymbiont‐mediated thelytoky in Megastigmus and its possible connections to host plant specialization. We demonstrate that thelytoky evolved from ancestral arrhenotoky through the horizontal transmission and the fixation of the parthenogenesis‐inducing Wolbachia. We find that ecological specialization in Wolbachia's hosts was probably a critical driving force for Wolbachia infection and spread of thelytoky, but also a constraint. Our work further reinforces the hypothesis that community structure of insects is a major driver of the epidemiology of endosymbionts and that competitive interactions among closely related species may facilitate their horizontal transmission.     

The kin selection theory of genomic imprinting and modes of reproduction in the eusocial Hymenoptera

Genomic imprinting is known from flowering plants and mammals but has not been confirmed for the Hymenoptera even though the eusocial Hymenoptera are prime candidates for this peculiar form of gene expression. Here, the kin selection theory of genomic imprinting is reviewed and applied to the eusocial Hymenoptera. The evidence for imprinting in eusocial Hymenoptera with the typical mode of reproduction, involving the sexual production of diploid female offspring, which develop into workers or gynes, and the arrhenotokous parthenogenesis of haploid males, is also reviewed briefly. However, the focus of this review is how atypical modes of reproduction, involving thelytokous parthenogenesis, hybridisation and androgenesis, may also select for imprinting. In particular, naturally occurring hybridisation in several genera of ants may provide useful tests of the role of kin selection in the evolution of imprinting. Hybridisation is expected to disrupt the coadaptation of antagonistically imprinted loci, and thus affect the phenotypes of hybrids. Some of the limited data available on hybrid worker reproduction and on colony sex ratios support predictions about patterns of imprinting derived from kin selection theory.