Perspective: maternal kin groups and the origins of asymmetric genetic systems-genomic imprinting, haplodiploidy, and parthenogenesis

The genetic systems of animals and plants are typically eumendelian. That is, an equal complement of autosomes is inherited from each of two parents, and at each locus, each parent's allele is equally likely to be expressed and equally likely to be transmitted. Genetic systems that violate any of these eumendelian symmetries are termed asymmetric and include parent-specific gene expression (PSGE), haplodiploidy, thelytoky, and related systems. Asymmetric genetic systems typically arise in lineages with close associations between kin (gregarious siblings, brooding, or viviparity). To date, different explanatory frameworks have been proposed to account for each of the different asymmetric genetic systems. Haig's kinship theory of genomic imprinting argues that PSGE arises when kinship asymmetries between interacting kin create conflicts between maternally and paternally derived alleles. Greater maternal than paternal relatedness within groups selects for more "abstemious" expression of maternally derived alleles and more "greedy" expression of paternally derived alleles. Here, I argue that this process may also underlie origins of haplodiploidy and many origins of thelytoky. The tendency for paternal alleles to be more "greedy" in maternal kin groups means that maternal-paternal conflict is not a zero-sum game: the maternal optimum will more closely correspond to the optimum for family groups and demes and for associated entities such as symbionts. Often in these circumstances, partial or complete suppression of paternal gene expression will evolve (haplodiploidy, thelytoky), or other features of the life cycle will evolve to minimize the conflict (monogamy, inbreeding). Maternally transmitted cytoplasmic elements and maternally imprinted nuclear alleles have a shared interest in minimizing agonistic interactions between female siblings and may cooperate to exclude the paternal genome. Eusociality is the most dramatic expression of the conflict-reducing effects of haplodiploidy, but its original and more widespread function may be suppression of intrafamilial cannibalism. In rare circumstances in which paternal gene products gain access to maternal physiology via a placenta, PSGE with greedy paternal gene expression can persist (e.g., in mammals).     

Absence of Wolbachia in Nonfilariid Nematodes

Intracellular bacteria of the genus Wolbachia are among the most abundant endosymbionts on the planet, occurring in at least two major phyla-the Arthropoda and Nematoda. Current surveys of Wolbachia distribution have found contrasting patterns within these groups. Whereas Wolbachia are widespread and occur in all three major subphyla of arthropods, with estimates placing them in at least several million arthropod species, the presence of nematodes carrying Wolbachia is currently confined to the filariids, in which they occur at appreciable frequencies. It has been hypothesized that Wolbachia entered the ancestor of modern-day filariids in a single acquisition event, and subsequently cospeciated with their filariid hosts. To further investigate this hypothesis, we examined the broader distribution of Wolbachia in nematodes using a polymerase chain reaction (PCR) assay in a diverse set of nonfilariid species. The assay consisted of three different types of PCR screens on adults of 20 secernentean nematode species (14 rhabditids, 2 strongylid parasites of vertebrates; 1 diplogasterid; 3 cephalobid relatives, 1 myolaim, and 1 filariid) and two adenophorean species (plectids). Two PCR screens were specific to the 16S rDNA and ftsZ protein coding gene of Wolbachia; and the third screen was specific to the 18S rDNA of the nematodes. Based upon our results, we conclude that Wolbachia are absent in all 21 non-filariid species encompassing all the major groups of the Secernentea and two species of Adenophorea, from which the Secernentea derived. The absence of Wolbachia in these non-filariids is consistent with the hypothesis that Wolbachia entered the nematode phylum once, in an ancestral lineage of extant filariids.     

Genomic conflict in scale insects: the causes and consequences of bizarre genetic systems

It is now clear that mechanisms of sex determination are extraordinarily labile, with considerable variation across all taxonomic levels. This variation is often expressed through differences in the genetic system (XX‐XY, XX‐XO, haplodiploidy, and so on). Why there is so much variation in such a seemingly fundamental process has attracted much attention, with recent ideas concentrating on the possible role of genomic conflicts of interest. Here we consider the role of inter‐ and intra‐genomic conflicts in one large insect taxon: the scale insects. Scale insects exhibit a dizzying array of genetic systems, and their biology promotes conflicts of interest over transmission and sex ratio between male‐ and female‐expressed genes, parental‐ and offspring‐expressed genes (both examples of intra‐genomic conflict) and between scale insects and their endosymbionts (inter‐genomic conflict). We first review the wide range of genetic systems found in scale insects and the possible evolutionary transitions between them. We then outline the theoretical opportunities for genomic conflicts in this group and how these might influence sex determination and sex ratio. We then consider the evidence for these conflicts in the evolution of sex determination in scale insects. Importantly, the evolution of novel genetic systems in scale insects has itself helped create new conflicts of interest, for instance over sex ratio. As a result, a major obstacle to our understanding of the role of conflict in the evolution of sex‐determination and genetic systems will be the difficulty in identifying the direction of causal relationships. We conclude by outlining possible experimental and comparative approaches to test more effectively how important genomic conflicts have been.     

The genetics and evolution of obligate reproductive parasitism in Trichogramma pretiosum infected with parthenogenesis-inducing Wolbachia

Parthenogenesis-inducing (PI) Wolbachia belong to a class of intracellular symbionts that distort the offspring sex ratio of their hosts toward a female bias. In many PI Wolbachia-infected species sex ratio distortion has reached its ultimate expression-fixation of infection and all-female populations. This is only possible with thelytokous PI symbionts as they provide an alternative form of reproduction and remove the requirement for males and sexual reproduction. Many populations fixed for PI Wolbachia infection have lost the ability to reproduce sexually, even when cured of the infection. We examine one such population in the species Trichogramma pretiosum. Through a series of backcrossing experiments with an uninfected Trichogramma pretiosum population we were able to show that the genetic basis for the loss of female sexual function could be explained by a dominant nuclear effect. Male sexual function had not been completely lost, though some deterioration of male sexual function was also evident when males from the infected population (created through antibiotic curing of infected females) were mated to uninfected females. We discuss the dynamics of sex ratio selection in PI Wolbachia-infected populations and the evolution of non-fertilizing mutations.     

Monitoring long-term evolutionary changes following Wolbachia introduction into a novel host: the Wolbachia popcorn infection in Drosophila simulans

Wolbachia may act as a biological control agent for pest management; in particular, the Wolbachia variant wMelPop (popcorn) shortens host longevity and may be useful for dengue suppression. However, long-term changes in the host and Wolbachia genomes can alter Wolbachia spread and/or host effects that suppress disease. Here, we investigate the phenotypic effects of wMelPop in a non-native host, Drosophila simulans, following artificial transinfection approximately 200 generations ago. Long-term rearing and maintenance of the bacteria were at 19°C in the original I-102 genetic background that was transinfected with the popcorn strain. The bacteria were then introgressed into three massbred backgrounds, and tetracycline was used to create uninfected sublines. The effect of wMelPop on longevity in this species appears to have changed; longevity was no longer reduced at 25°C in some nuclear backgrounds, reflecting different geographical origin, selection or drift, although the reduction was still evident for flies held at 30°C. Wolbachia influenced productivity and viability, and development time in some host backgrounds. These findings suggest that long-term attenuation of Wolbachia effects may compromise the effectiveness of this bacterium in pest control. They also emphasize the importance of host nuclear background on Wolbachia phenotypic effects.     

The dynamic relationship between polyandry and selfish genetic elements

Selfish genetic elements (SGEs) are ubiquitous in eukaryotes and bacteria, and make up a large part of the genome. They frequently target sperm to increase their transmission success, but these manipulations are often associated with reduced male fertility. Low fertility of SGE-carrying males is suggested to promote polyandry as a female strategy to bias paternity against male carriers. Support for this hypothesis is found in several taxa, where SGE-carrying males have reduced sperm competitive ability. In contrast, when SGEs give rise to reproductive incompatibilities between SGE-carrying males and females, polyandry is not necessarily favoured, irrespective of the detrimental impact on male fertility. This is due to the frequency-dependent nature of these incompatibilities, because they will decrease in the population as the frequency of SGEs increases. However, reduced fertility of SGE-carrying males can prevent the successful population invasion of SGEs. In addition, SGEs can directly influence male and female mating behaviour, mating rates and reproductive traits (e.g. female reproductive tract length and male sperm). This reveals a potent and dynamic interaction between SGEs and polyandry highlighting the potential to generate sexual selection and conflict, but also indicates that polyandry can promote harmony within the genome by undermining the spread of SGEs.     

Occasional males in parthenogenetic populations of Asobara japonica (Hymenoptera: Braconidae): low Wolbachia titer or incomplete coadaptation?

Wolbachia are endosymbiotic bacteria known to manipulate the reproduction of their hosts. Some populations of the parasitoid wasp Asobara japonica are infected with Wolbachia and reproduce parthenogenetically, while other populations are not infected and reproduce sexually. Wolbachia-infected A. japonica females regularly produce small numbers of male offspring. Because all females in the field are infected and infected females are not capable of sexual reproduction, male production seems to be maladaptive. We investigated why these females nevertheless produce males. We tested three hypotheses: high rearing temperatures could result in higher offspring sex ratios (more males), low Wolbachia titer of the mother could lead to higher offspring sex ratios and/or the Wolbachia infection is of relatively recent origin and not enough time has passed to allow complete coadaptation between Wolbachia and host. In all, 33% of the Wolbachia-infected females produced males and 56% of these males were also infected with Wolbachia. Neither offspring sex ratio nor male infection frequency was significantly affected by rearing temperature or Wolbachia concentration of the mother. The mitochondrial DNA sequence of one of the uninfected populations was identical to that of two of the infected populations. Therefore, the initial Wolbachia infection of A. japonica must have occurred recently. Mitochondrial sequence variation among the infected populations suggests that the spread of Wolbachia through the host populations involved horizontal transmission. We conclude that the occasional male production by Wolbachia-infected females is most likely a maladaptive side effect of incomplete coevolution between symbiont and host in this relatively young infection.     

Genetic analyses reveal independent domestication origins of Eurasian reindeer

Although there is little doubt that the domestication of mammals was instrumental for the modernization of human societies, even basic features of the path towards domestication remain largely unresolved for many species. Reindeer are considered to be in the early phase of domestication with wild and domestic herds still coexisting widely across Eurasia. This provides a unique model system for understanding how the early domestication process may have taken place. We analysed mitochondrial sequences and nuclear microsatellites in domestic and wild herds throughout Eurasia to address the origin of reindeer herding and domestication history. Our data demonstrate independent origins of domestic reindeer in Russia and Fennoscandia. This implies that the Saami people of Fennoscandia domesticated their own reindeer independently of the indigenous cultures in western Russia. We also found that augmentation of local reindeer herds by crossing with wild animals has been common. However, some wild reindeer populations have not contributed to the domestic gene pool, suggesting variation in domestication potential among populations. These differences may explain why geographically isolated indigenous groups have been able to make the technological shift from mobile hunting to large-scale reindeer pastoralism independently.     

Stochastic spread of Wolbachia

Wolbachia are very common, maternally transmitted endosymbionts of insects. They often spread by a mechanism termed cytoplasmic incompatibility (CI) that involves reduced egg hatch when Wolbachia-free ova are fertilized by sperm from Wolbachia-infected males. Because the progeny of Wolbachia-infected females generally do not suffer CI-induced mortality, infected females are often at a reproductive advantage in polymorphic populations. Deterministic models show that Wolbachia that impose no costs on their hosts and have perfect maternal transmission will spread from arbitrarily low frequencies (though initially very slowly); otherwise, there will be a threshold frequency below which Wolbachia frequencies decline to extinction and above which they increase to fixation or a high stable equilibrium. Stochastic theory was used to calculate the probability of fixation in populations of different size for arbitrary current frequencies of Wolbachia, with special attention paid to the case of spread after the arrival of a single infected female. Exact results are given based on a Moran process that assumes a specific demographic model, and approximate results are obtained using the more general Wright-Fisher theory. A new analytical approximation for the probability of fixation is derived, which performs well for small population sizes. The significance of stochastic effects in the natural spread of Wolbachia and their relevance to the use of Wolbachia as a drive mechanism in vector and pest management are discussed.     

Sexually antagonistic genetic variance for fitness in an ancestral and a novel environment

The intersex genetic correlation for fitness (rwfm), a standardized measure of the degree to which male and female fitness covary genetically, has consequences for important evolutionary processes, but few estimates are available and none have explored how it changes with environment. Using a half-sibling breeding design, we estimated the genetic (co)variance matrix (G) for male and female fitness, and the resulting rwfm, in Drosophila serrata. Our estimates were performed in two environments: the laboratory yeast food to which the population was well adapted and a novel corn food. The major axis of genetic variation for fitness in the two environments, accounting for 51.3 per cent of the total genetic variation, was significant and revealed a strong signal of sexual antagonism, loading negatively in both environments on males but positively on females. Consequently, estimates of rwfm were negative in both environments (−0.34 and −0.73, respectively), indicating that the majority of genetic variance segregating in this population has contrasting effects on male and female fitness. The possible strengthening of the negative rwfm in this novel environment may be a consequence of no history of selection for amelioration of sexual conflict. Additional studies from a diverse range of novel environments will be needed to determine the generality of this finding.     

Disrupting the timing of Wolbachia-induced male-killing

Several lineages of maternally inherited symbionts have evolved the ability to kill infected females' sons, a phenomenon known as male-killing. Male-killing varies in its timing, from early (death during embryogenesis) to late (mortality of late larval instars). Following the observation that treatment of male-killer infected adult females Hypolimnas bolina with tetracycline, a bacteriostatic antibiotic, produces a delay in the timing of male death, we hypothesized that early male-killers possess the ability to kill males through bacterial activity outside of embryogenesis. We verified this hypothesis by showing that treatment of surviving larvae with the bacteriocidal antibiotic rifampicin rescues males. This discounted the hypothesis that delayed death occurred due to postponed effects of toxins produced at earlier stages, and thus supported the importance of bacterial activity in the larval phase in delayed male-killing. These results argue against the view that early male-killing is achieved by specifically targeting an early developmental process within the sex determination pathway.     

Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts

The life cycles of many organisms are constrained by the seasonality of resources. This is particularly true for leaf-mining herbivorous insects that use deciduous leaves to fuel growth and reproduction even beyond leaf fall. Our results suggest that an intimate association with bacterial endosymbionts might be their way of coping with nutritional constraints to ensure successful development in an otherwise senescent environment. We show that the phytophagous leaf-mining moth Phyllonorycter blancardella (Lepidoptera) relies on bacterial endosymbionts, most likely Wolbachia, to manipulate the physiology of its host plant resulting in the ‘green-island’ phenotype—photosynthetically active green patches in otherwise senescent leaves—and to increase its fitness. Curing leaf-miners of their symbiotic partner resulted in the absence of green-island formation on leaves, increased compensatory larval feeding and higher insect mortality. Our results suggest that bacteria impact green-island induction through manipulation of cytokinin levels. This is the first time, to our knowledge, that insect bacterial endosymbionts have been associated with plant physiology.     

Population genetic structure of sexual and parthenogenetic damselflies inferred from mitochondrial and nuclear markers

It has been postulated that obligate asexual lineages may persist in the long term if they escape from negative interactions with either sexual lineages or biological enemies; and thus, parthenogenetic populations will be more likely to occur in places that are difficult for sexuals to colonize, or those in which biological interactions are rare, such as islands or island-like habitats. Ischnura hastata is the only known example of natural parthenogenesis within the insect order Odonata, and it represents also a typical example of geographic parthenogenesis, as sexual populations are widely distributed in North America, whereas parthenogenetic populations of this species have only been found at the Azores archipelago. In order to gain insight in the origin and distribution of parthenogenetic I. hastata lineages, we have used microsatellites, mitochondrial and nuclear DNA sequence data, to examine the population genetic structure of this species over a wide geographic area. Our results suggest that sexual populations of I. hastata in North America conform to a large subdivided population that has gone through a recent spatial expansion. A recent single long distance dispersal event, followed by a demographic expansion, is the most parsimonious hypothesis explaining the origin of the parthenogenetic population of this species in the Azores islands.     

The alignment between phenotypic plasticity,the major axis of genetic variation and the response to selection

Phenotypic plasticity is the ability of a genotype to produce more than one phenotype in order to match the environment. Recent theory proposes that the major axis of genetic variation in a phenotypically plastic population can align with the direction of selection. Therefore, theory predicts that plasticity directly aids adaptation by increasing genetic variation in the direction favoured by selection and reflected in plasticity. We evaluated this theory in the freshwater crustacean Daphnia pulex, facing predation risk from two contrasting size-selective predators. We estimated plasticity in several life-history traits, the G matrix of these traits, the selection gradients on reproduction and survival, and the predicted responses to selection. Using these data, we tested whether the genetic lines of least resistance and the predicted response to selection aligned with plasticity. We found predator environment-specific G matrices, but shared genetic architecture across environments resulted in more constraint in the G matrix than in the plasticity of the traits, sometimes preventing alignment of the two. However, as the importance of survival selection increased, the difference between environments in their predicted response to selection increased and resulted in closer alignment between the plasticity and the predicted selection response. Therefore, plasticity may indeed aid adaptation to new environments.     

Genetic Variation of Taenia Pisiformis Collected from Sichuan,China, Based on the Mitochondrial Cytochrome b gene

Taenia pisiformis is one of the most important parasites of canines and rabbits. T. pisiformis cysticercus (the larval stage) causes severe damage to rabbit breeding, which results in huge economic losses. In this study, the genetic variation of T. pisiformis was determined in Sichuan Province, China. Fragments of the mitochondrial cytochrome b (cytb) (922 bp) gene were amplified in 53 isolates from 8 regions of T. pisiformis. Overall, 12 haplotypes were found in these 53 cytb sequences. Molecular genetic variations showed 98.4% genetic variation derived from intra-region. F_ST and Nm values suggested that 53 isolates were not genetically differentiated and had low levels of genetic diversity. Neutrality indices of the cytb sequences showed the evolution of T. pisiformis followed a neutral mode. Phylogenetic analysis revealed no correlation between phylogeny and geographic distribution. These findings indicate that 53 isolates of T. pisiformis keep a low genetic variation, which provide useful knowledge for monitoring changes in parasite populations for future control strategies.     

Genetic diversity and genetic relationships in Hyacinthaceae in India using RAPD and SRAP markers

Genetic diversity and relationship among three genera namely Drimia, Dipcadi and Ledebouria of Hyacinthaceae in India was studied using RAPD and SRAP markers. Twenty one RAPD primers and nine SRAP were used for analyzing 41 accessions. RAPD gave an average 12.6 markers per primer, while SRAP generated 10.1 markers per primer pair. The family emerged very diverged with high polymorphism. The study resolved the three genera into monophyletic groups corresponding to three subfamilies; Urginoideae, Hyacinthoideae and Ornithogaloideae. Drimia wightii emerged a very distinct species and species specific markers were obtained with both marker systems. AMOVA analysis also revealed the genera to be quite well diverged. The two markers showed high correlation (r = 0.932) in Mantel matrix crresspondance test. The combined data also showed a very good correlation with the respective markers individually.     

Genetic diversity and structure in two species of Leavenworthia with self-incompatible and self-compatible populations

Self-fertilization is a common mating system in plants and is known to reduce genetic diversity, increase genetic structure and potentially put populations at greater risk of extinction. In this study, we measured the genetic diversity and structure of two cedar glade endemic species, Leavenworthia alabamica and L. crassa. These species have self-incompatible (SI) and self-compatible (SC) populations and are therefore ideal for understanding how the mating system affects genetic diversity and structure. We found that L. alabamica and L. crassa had high species-level genetic diversity (H_e=0.229 and 0.183, respectively) and high genetic structure among their populations (F_ST=0.45 and 0.36, respectively), but that mean genetic diversity was significantly lower in SC compared with SI populations (SC vs SI, H_e for L. alabamica was 0.065 vs 0.206 and for L. crassa was 0.084 vs 0.189). We also found significant genetic structure using maximum-likelihood clustering methods. These data indicate that the loss of SI leads to the loss of genetic diversity within populations. In addition, we examined genetic distance relationships between SI and SC populations to analyze possible population history and origins of self-compatibility. We find there may have been multiple origins of self-compatibility in L. alabamica and L. crassa. However, further work is required to test this hypothesis. Finally, given their high genetic structure and that individual populations harbor unique alleles, conservation strategies seeking to maximize species-level genetic diversity for these or similar species should protect multiple populations.     

Identification of Wolbachia-responsive microRNAs in the two-spotted spider mite,Tetranychus urticae

Background

The two-spotted spider mite, Tetranychus urticae, is infected with Wolbachia, which have the ability to manipulate host reproduction and fitness. MicroRNAs (miRNAs) are small non-coding RNAs that are involved in many biological processes such as development, reproduction and host-pathogen interactions. Although miRNA was observed to involve in Wolbachia-host interactions in the other insect systems, its roles have not been fully deciphered in the two-spotted spider mite.

Results

Small RNA libraries of infected and uninfected T. urticae for both sexes (in total four libraries) were constructed. By integrating the mRNA data originated from the same samples, the target genes of the differentially expressed miRNAs were predicted. Then, GO and pathway analyses were performed for the target genes. Comparison of libraries showed that Wolbachia infection significantly regulated 91 miRNAs in females and 20 miRNAs in males, with an overall suppression of miRNAs in Wolbachia-infected libraries. A comparison of the miRNA and mRNA data predicted that the differentially expressed miRNAs negatively regulated 90 mRNAs in females and 9 mRNAs in males. An analysis of target genes showed that Wolbachia-responsive miRNAs regulated genes with function in sphingolipid metabolism, lysosome function, apoptosis and lipid transporting in both sexes, as well as reproduction in females.

Conclusion

Comparisons of the miRNA and mRNA data can help to identify miRNAs and miRNA target genes involving in Wolbachia-host interactions. The molecular targets identified in this study should be useful in further functional studies.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-1122) contains supplementary material, which is available to authorized users.     

High levels of genetic differentiation and selfing in the Brazilian cerrado fruit tree Dipteryx alata Vog. (Fabaceae)

Dipteryx alata is a native fruit tree species of the cerrado (Brazilian savanna) that has great economic potential because of its multiple uses. Knowledge of how the genetic variability of this species is organized within and among populations would be useful for genetic conservation and breeding programs. We used nine simple sequence repeat (SSR) primers developed for Dipteryx odorata to evaluate the genetic structure of three populations of D. alata located in central Brazil based on a leaf sample analysis from 101 adults. The outcrossing rate was evaluated using 300 open-pollinated offspring from 25 seed-trees. Pollen dispersal was measured by parentage analysis. We used spatial genetic structure (SGS) to test the minimal distance for harvesting seeds in conservation and breeding programs. Our data indicate that the populations studied had a high degree of genetic diversity and population structure, as suggested by the high level of divergence among populations . The estimated outcrossing rate suggested a mixed mating system, and the intrapopulation fixation index was influenced by SGS. We conclude that seed harvesting for genetic conservation and breeding programs requires a minimum distance between trees of 196 m to avoid collecting seeds from related seed-trees.     

Scaling of processes shaping the clonal dynamics and genetic mosaic of seagrasses through temporal genetic monitoring

Theoretically, the dynamics of clonal and genetic diversities of clonal plant populations are strongly influenced by the competition among clones and rate of seedling recruitment, but little empirical assessment has been made of such dynamics through temporal genetic surveys. We aimed to quantify 3 years of evolution in the clonal and genetic composition of Zostera marina meadows, comparing parameters describing clonal architecture and genetic diversity at nine microsatellite markers. Variations in clonal structure revealed a decrease in the evenness of ramet distribution among genets. This illustrates the increasing dominance of some clonal lineages (multilocus lineages, MLLs) in populations. Despite the persistence of these MLLs over time, genetic differentiation was much stronger in time than in space, at the local scale. Contrastingly with the short-term evolution of clonal architecture, the patterns of genetic structure and genetic diversity sensu stricto (that is, heterozygosity and allelic richness) were stable in time. These results suggest the coexistence of (i) a fine grained (at the scale of a 20 × 30 m quadrat) stable core of persistent genets originating from an initial seedling recruitment and developing spatial dominance through clonal elongation; and (ii) a local (at the scale of the meadow) pool of transient genets subjected to annual turnover. This simultaneous occurrence of initial and repeated recruitment strategies highlights the different spatial scales at which distinct evolutionary drivers and mating systems (clonal competition, clonal growth, propagule dispersal and so on) operate to shape the dynamics of populations and the evolution of polymorphism in space and time.