Female and male genetic contributions to post-mating immune defence in female Drosophila melanogaster

Post-mating reduction in immune defence is common in female insects, and a trade-off between mating and immunity could affect the evolution of immunity. In this work, we tested the capacity of virgin and mated female Drosophila melanogaster to defend against infection by four bacterial pathogens. We found that female D. melanogaster suffer post-mating immunosuppression in a pathogen-dependent manner. The effect of mating was seen after infection with two bacterial pathogens (Providencia rettgeri and Providencia alcalifaciens), though not after infection with two other bacteria (Enterococcus faecalis and Pseudomonas aeruginosa). We then asked whether the evolution of post-mating immunosuppression is primarily a ‘female’ or ‘male’ trait by assaying for genetic variation among females for the degree of post-mating immune suppression they experience and among males for the level of post-mating immunosuppression they elicit in their mates. We also assayed for an interaction between male and female genotypes to test the specific hypothesis that the evolution of a trade-off between mating and immune defence in females might be being driven by sexual conflict. We found that females, but not males, harbour significant genetic variation for post-mating immunosuppression, and we did not detect an interaction between female and male genotypes. We thus conclude that post-mating immune depression is predominantly a ‘female’ trait, and find no evidence that it is evolving under sexual conflict.     

Sexual deception in a cannibalistic mating system? Testing the Femme Fatale hypothesis

Animal communication theory holds that in order to be evolutionarily stable, signals must be honest on average, but significant dishonesty (i.e. deception) by a subset of the population may also evolve. A typical praying mantid mating system involves active mate searching by males, which is guided by airborne sex pheromones in most species for which mate-searching cues have been studied. The Femme Fatale hypothesis suggests that female mantids may be selected to exploit conspecific males as prey if they benefit nutritionally from cannibalism. Such a benefit exists in the false garden mantid Pseudomantis albofimbriata—females use the resources gained from male consumption to significantly increase their body condition and reproductive output. This study aimed to examine the potential for chemical deception among the subset of females most likely to benefit from cannibalism (poorly fed females). Females were placed into one of four feeding treatments (‘Very Poor’, ‘Poor’, ‘Medium’ and ‘Good’), and males were given the opportunity to choose between visually obscured females in each of the treatments. Female body condition and fecundity varied linearly with food quantity; however, female attractiveness did not. That is, Very Poor females attracted significantly more males than any of the other female treatments, even though these females were in significantly poorer condition, less fecund (in this study) and more likely to cannibalise (in a previous study). In addition, there was a positive correlation between fecundity and attractiveness if Very Poor females were removed from the analysis, suggesting an inherently honest signalling system with a subset of dishonest individuals. This is the first empirical study to provide evidence of sexual deception via chemical cues, and the first to provide support for the Femme Fatale hypothesis.     

Size-dependent alternative male mating tactics in the yellow dung fly,Scathophaga stercoraria

Whenever males can monopolize females and/or resources used by females, the opportunity for sexual selection will be great. The greater the variation among males in reproductive success, the greater the intensity of selection on less competitive males to gain matings through alternative tactics. In the yellow dung fly, Scathophaga stercoraria, males aggressively compete for access to receptive, gravid females on fresh dung. Larger males are better able to acquire mates and to complete copulation successfully and guard the female throughout oviposition. Here we demonstrate that when an alternative resource is present where females aggregate (i.e. apple pomace, where both sexes come to feed), smaller males will redirect their searching for females from dung to the new substrate. In addition, we identify a class of particularly small males on the alternative substrate that appears never to be present searching for females on or around dung. Smaller males were found to have a mating ‘advantage’ on pomace, in striking contrast to the pattern observed on dung, providing further support for the existence of an alternative male reproductive tactic in this species.     

Unravelling the Wolbachia evolutionary role: the reprogramming of the host genomic imprinting

Environmental factors can induce significant epigenetic changes that may also be inherited by future generations. The maternally inherited symbiont of arthropods Wolbachia pipientis is an excellent candidate as an ‘environmental’ factor promoting trans-generational epigenetic changes: by establishing intimate relationships with germ-line cells, epigenetic effects of Wolbachia symbiosis would be manifested as a ‘maternal effect’, in which infection of the mother modulates the offspring phenotype. In the leafhopper Zyginidia pullula, Wolbachia feminizes genetic males, leaving them as intersexes. With the exception of male chitinous structures that are present in the last abdominal segment, feminized males display phenotypic features that are typical of females. These include ovaries that range from a typical histological architecture to an altered structure. Methylation-sensitive random amplification of polymorphic DNA profiles show that they possess a female genomic imprint. On the other hand, some rare feminized males bear testes instead of ovaries. These specimens possess a Wolbachia density approximately four orders of magnitude lower than feminized males with ovaries and maintain a male genome—methylation pattern. Our results indicate that Wolbachia infection disrupts male imprinting, which dramatically influences the expression of genes involved in sex differentiation and development, and the alteration occurs only if Wolbachia exceeds a density threshold. Thus, a new Wolbachia''s role as an environmental evolutionary force, inducing epigenetic trans-generational changes, should now be considered.     

Male genotype influences female reproductive investment in Drosophila melanogaster

In many species, males can influence the amount of resources their mates invest in reproduction. Two favoured hypotheses for this observation are that females assess male quality during courtship or copulation and alter their investment in offspring accordingly, or that males manipulate females to invest heavily in offspring produced soon after mating. Here, we examined whether there is genetic variation for males to influence female short-term reproductive investment in Drosophila melanogaster, a species with strong sexual selection and substantial sexual conflict. We measured the fecundity and egg size of females mated to males from multiple isofemale lines collected from populations around the globe. Although these traits were not strongly influenced by the male's population of origin, we found that 22 per cent of the variation in female short-term reproductive investment was attributable to the genotype of her mate. This is the first direct evidence that male D. melanogaster vary genetically in their proximate influence on female fecundity, egg size and overall reproductive investment.     

Environmental transmission of a personality trait: foster parent exploration behaviour predicts offspring exploration behaviour in zebra finches

Consistent behavioural differences among individuals are common in many species and can have important effects on offspring fitness. To understand such ‘personality’ variation, it is important to determine the mode of inheritance, but this has been quantified for only a few species. Here, we report results from a breeding experiment in captive zebra finches, Taeniopygia guttata, in which we cross-fostered offspring to disentangle the importance of genetic and non-genetic transmission of behaviour. Genetic and foster-parents’ exploratory type was measured in a novel environment pre-breeding and offspring exploratory type was assessed at adulthood. Offspring exploratory type was predicted by the exploratory behaviour of the foster but not the genetic parents, whereas offspring size was predicted by genetic but not foster-parents’ size. Other aspects of the social environment, such as rearing regime (uni- versus biparental), hatching position, brood size or an individual''s sex did not influence offspring exploration. Our results therefore indicate that non-genetic transmission of behaviour can play an important role in shaping animal personality variation.     

Albinism in phylogenetically and geographically distinct populations of Astyanax cavefish arises through the same loss-of-function Oca2 allele

The Mexican tetra, Astyanax mexicanus, comprises 29 populations of cave-adapted fish distributed across a vast karst region in northeastern Mexico. These populations have a complex evolutionary history, having descended from ‘old'' and ‘young'' ancestral surface-dwelling stocks that invaded the region ∼6.7 and ∼2.8 MYa, respectively. This study investigates a set of captive, pigmented Astyanax cavefish collected from the Micos cave locality in 1970, in which albinism appeared over the past two decades. We combined novel coloration analyses, coding sequence comparisons and mRNA expression level studies to investigate the origin of albinism in captive-bred Micos cavefish. We discovered that albino Micos cavefish harbor two copies of a loss-of-function ocular and cutaneous albinism type II (Oca2) allele previously identified in the geographically distant Pachón cave population. This result suggests that phylogenetically young Micos cavefish and phylogenetically old Pachón cave fish inherited this Oca2 allele from the ancestral surface-dwelling taxon. This likely resulted from the presence of the loss-of-function Oca2 haplotype in the ‘young'' ancestral surface-dwelling stock that colonized the Micos cave and also introgressed into the ancient Pachón cave population. The appearance of albinism in captive Micos cavefish, caused by the same loss-of-function allele present in Pachón cavefish, implies that geographically and phylogenetically distinct cave populations can evolve the same troglomorphic phenotype from standing genetic variation present in the ancestral taxon.     

Does coping style predict optimization? An experimental test in a wild passerine bird

A number of studies have suggested that avian brood size is individually optimized. Yet, optimal reproductive decisions likely vary owing to among-individual differences in environmental sensitivity. Specifically, ‘proactive’ individuals who do not track environmental changes may be less able to produce optimal brood sizes than ‘reactive’ individuals who have more precise local environmental knowledge. To test this, we quantified exploratory behaviour (a proxy for proactivity) in a great tit (Parus major) population, manipulated brood sizes (reduced, control, enlarged) and evaluated whether individuals of dissimilar coping style differed in their level of optimization. If reactive females behaved optimally, any deviation from their original brood size should lower fitness, whereas this should not be the case for proactive females. Reactive females indeed performed best at their natural brood size, whereas proactive females performed best when raising an enlarged brood. These findings imply that proactive females produced sub-optimal brood sizes. We speculate that proactive females might (i) take decisions based on biased perception of their environment, (ii) face energetic constraints in offspring production and/or (iii) be more willing to invest into current reproduction when given the option. Our findings provide experimental evidence for coping style-related differences in optimal reproductive decisions and life-history strategies.     

Does egg carotenoid improve larval quality in Arctic charr (Salvelinus alpinus)?

Females in mutually ornamented species are often less conspicuously ornamented than their male conspecifics. It has been hypothesized that offspring quality may decrease if females invest more resources into ornaments at the expense of resources in eggs. An experiment was carried out to test whether natural variation in carotenoid in the eggs from a wild population of Arctic charr (Salvelinus alpinus) was associated with survival and growth of their offspring until hatching. Wild Arctic charr were caught at a spawning ground during the spawning period. Eggs from two different females, one female with yellowish carotenoid‐rich eggs and one with paler eggs, were fertilized by sperm from the same male. This was repeated until gametes were collected from 42 females and 21 males, giving a total of 21 groups. After fertilization, the zygotes from each of the two females were reared in four replicated groups. These 168 groups were reared separately until hatching when the surviving larvae were counted and their body length measured. For the two response variables survival and body length at hatching, no effect was demonstrated of any of the predictors (i) amount of carotenoid in the unfertilized eggs, (ii) the mothers'' body condition, or (iii) ornament intensity of their red carotenoid‐based abdominal ornament. Thus, this study gives no support for the hypothesis that females investing less carotenoid into their eggs suffer from decreased offspring quality until hatching. This lack of association between female ornament intensity and their fitness is not as expected if female ornaments evolved due to direct sexual selection from males on the more ornamented females (“direct selection hypothesis”).     

Sickness behaviour acting as an evolutionary trap? Male house finches preferentially feed near diseased conspecifics

Host behaviour towards infectious conspecifics is a crucial yet overlooked component of pathogen dynamics. Selection is expected to favour individuals who can recognize and avoid infected conspecifics in order to reduce their own risk of infection. However, evidence is scarce and limited to species employing chemical cues. Here, we experimentally examine whether healthy captive house finches (Carpodacus mexicanus) preferentially forage near a same-sex, healthy conspecific versus one infected with the directly transmissible pathogen Mycoplasma gallisepticum (MG), which causes lethargy and visible conjunctivitis. Interestingly, male house finches strongly preferred feeding near diseased conspecifics, while females showed no preference. This sex difference appeared to be the result of lower aggression rates in diseased males, but not in females. The reduced aggression of diseased males may act as an ‘evolutionary trap’ by presenting a historically beneficial behavioural cue in the context of a new environment, which now includes a recently emerged, potentially fatal pathogen. Since MG can be directly transmitted during feeding, healthy males may inadvertently increase their risk of contracting MG. This behaviour is likely to significantly contribute to the continued persistence of MG epidemics in wild populations.     

The hawk–dove game in a sexually reproducing species explains a colourful polymorphism of an endangered bird

The hawk–dove game famously introduced strategic game theory thinking into biology and forms the basis of arguments for limited aggression in animal populations. However, aggressive ‘hawks’ and peaceful ‘doves’, with strategies inherited in a discrete manner, have never been documented in a real animal population. Thus, the applicability of game-theoretic arguments to real populations might be contested. Here, we show that the head-colour polymorphism of red and black Gouldian finches (Erythrura gouldiae) provides a real-life example. The aggressive red morph is behaviourally dominant and successfully invades black populations, but when red ‘hawks’ become too common, their fitness is severely compromised (via decreased parental ability). We also investigate the effects of real-life deviations, particularly sexual reproduction, from the simple original game, which assumed asexual reproduction. A protected polymorphism requires mate choice to be sufficiently assortative. Assortative mating is adaptive for individuals because of genetic incompatibilities affecting hybrid offspring fitness, but by allowing red ‘hawks’ to persist, it also leads to significantly reduced population sizes. Because reductions in male contributions to parental care are generally known to lead to lower population productivity in birds, we expect zero-sum competition to often have wide ranging population consequences.     

Pollen dispersal and gene flow within and into a population of the alpine monocarpic plant Campanula thyrsoides

Background and Aims

Gene flow by seed and pollen largely shapes the genetic structure within and among plant populations. Seed dispersal is often strongly spatially restricted, making gene flow primarily dependent on pollen dispersal within and into populations. To understand distance-dependent pollination success, pollen dispersal and gene flow were studied within and into a population of the alpine monocarpic perennial Campanula thyrsoides.

Methods

A paternity analysis was performed on sampled seed families using microsatellites, genotyping 22 flowering adults and 331 germinated offspring to estimate gene flow, and pollen analogues were used to estimate pollen dispersal. The focal population was situated among 23 genetically differentiated populations on a subalpine mountain plateau (<10 km²) in central Switzerland.

Key Results

Paternity analysis assigned 110 offspring (33·2 %) to a specific pollen donor (i.e. ‘father’) in the focal population. Mean pollination distance was 17·4 m for these offspring, and the pollen dispersal curve based on positive LOD scores of all 331 offspring was strongly decreasing with distance. The paternal contribution from 20–35 offspring (6·0–10·5 %) originated outside the population, probably from nearby populations on the plateau. Multiple potential fathers were assigned to each of 186 offspring (56·2 %). The pollination distance to ‘mother’ plants was negatively affected by the mothers'' degree of spatial isolation in the population. Variability in male mating success was not related to the degree of isolation of father plants.

Conclusions

Pollen dispersal patterns within the C. thyrsoides population are affected by spatial positioning of flowering individuals and pollen dispersal may therefore contribute to the course of evolution of populations of this species. Pollen dispersal into the population was high but apparently not strong enough to prevent the previously described substantial among-population differentiation on the plateau, which may be due to the monocarpic perenniality of this species.     

Females prefer to associate with males with longer intromittent organs in mosquitofish

Sexual selection is a major force behind the rapid evolution of male genital morphology among species. Most within-species studies have focused on sexual selection on male genital traits owing to events during or after copulation that increase a male''s share of paternity. Very little attention has been given to whether genitalia are visual signals that cause males to vary in their attractiveness to females and are therefore under pre-copulatory sexual selection. Here we show that, on average, female eastern mosquitofish Gambusia holbrooki spent more time in association with males who received only a slight reduction in the length of the intromittent organ (‘gonopodium’) than males that received a greater reduction. This preference was, however, only expressed when females chose between two large males; for small males, there was no effect of genital size on female association time.     

Age-dependent female responses to a male ejaculate signal alter demographic opportunities for selection

A central tenet of evolutionary explanations for ageing is that the strength of selection wanes with age. However, data on age-specific expression and benefits of sexually selected traits are lacking—particularly for traits subject to sexual conflict. We addressed this by using as a model the responses of Drosophila melanogaster females of different ages to receipt of sex peptide (SP), a seminal fluid protein transferred with sperm during mating. SP can mediate sexual conflict, benefitting males while causing fitness costs in females. Virgin and mated females of all ages showed significantly reduced receptivity in response to SP. However, only young virgin females also showed increased egg laying; hence, there was a narrow demographic window of maximal responses to SP. Males gained significant ‘per mating’ fitness benefits only when mating with young females. The pattern completely reversed in matings with older females, where SP transfer was costly. The overall benefits of SP transfer (hence opportunity for selection) therefore reversed with female age. The data reveal a new example of demographic variation in the strength of selection, with convergence and conflicts of interest between males and ageing females occurring over different facets of responses to a sexually antagonistic trait.     

Paleovirology of ‘syncytins’, retroviral env genes exapted for a role in placentation

The development of the emerging field of ‘paleovirology’ allows biologists to reconstruct the evolutionary history of fossil endogenous retroviral sequences integrated within the genome of living organisms and has led to the retrieval of conserved, ancient retroviral genes ‘exapted’ by ancestral hosts to fulfil essential physiological roles, syncytin genes being undoubtedly among the most remarkable examples of such a phenomenon. Indeed, syncytins are ‘new’ genes encoding proteins derived from the envelope protein of endogenous retroviral elements that have been captured and domesticated on multiple occasions and independently in diverse mammalian species, through a process of convergent evolution. Knockout of syncytin genes in mice provided evidence for their absolute requirement for placenta development and embryo survival, via formation by cell–cell fusion of syncytial cell layers at the fetal–maternal interface. These genes of exogenous origin, acquired ‘by chance’ and yet still ‘necessary’ to carry out a basic function in placental mammals, may have been pivotal in the emergence of mammalian ancestors with a placenta from egg-laying animals via the capture of a founding retroviral env gene, subsequently replaced in the diverse mammalian lineages by new env-derived syncytin genes, each providing its host with a positive selective advantage.     

Molecular Characterization of Barley 3H Semi-Dwarf Genes

The barley chromosome 3H accommodates many semi-dwarfing genes. To characterize these genes, the two-rowed semi-dwarf Chinese barley landrace ‘TX9425’ was crossed with the Australian barley variety ‘Franklin’ to generate a doubled haploid (DH) population, and major QTLs controlling plant height have been identified in our previous study. The major QTL derived from ‘TX9425’ was targeted to investigate the allelism of the semi-dwarf gene uzu in barley. Twelve sets of near-isogenic lines and a large NILF₂ fine mapping population segregating only for the dwarfing gene from ‘TX9425’ were developed. The semi-dwarfing gene in ‘TX9425’ was located within a 2.8 cM region close to the centromere on chromosome 3H by fine mapping. Molecular cloning and sequence analyses showed that the ‘TX9425’-derived allele contained a single nucleotide substitution from A to G at position 2612 of the HvBRI1 gene. This was apparently the same mutation as that reported in six-rowed uzu barley. Markers co-segregating with the QTL were developed from the sequence of the HvBRI1 gene and were validated in the ‘TX9425’/‘Franklin’ DH population. The other major dwarfing QTL derived from the Franklin variety was distally located on chromosome 3HL and co-segregated with the sdw1 diagnostic marker hv20ox2. A third dwarfing gene, expressed only in winter-sown trials, was identified and located on chromosome 3HS. The effects and interactions of these dwarfing genes under different growing conditions are discussed. These results improve our understanding of the genetic mechanisms controlling semi-dwarf stature in barley and provide diagnostic markers for the selection of semi-dwarfness in barley breeding programs.     

Drosophila male sex peptide inhibits siesta sleep and promotes locomotor activity in the post-mated female

Quiescence, or a sleep-like state, is a common and important feature of the daily lives of animals from both invertebrate and vertebrate taxa, suggesting that sleep appeared early in animal evolution. Recently, Drosophila melanogaster has been shown to be a relevant and powerful model for the genetic analysis of sleep behaviour. The sleep architecture of D. melanogaster is sexually dimorphic, with females sleeping much less than males during day-time, presumably because reproductive success requires greater foraging activity by the female as well as the search for egg-laying sites. However, this loss of sleep and increase in locomotor activity will heighten the risk for the female from environmental and predator hazards. In this study, we show that virgin females can minimize this risk by behaving like males, with an extended afternoon ‘siesta’. Copulation results in the female losing 70 per cent of day-time sleep and becoming more active. This behaviour lasts for at least 8 days after copulation and is abolished if the mating males lack sex peptide (SP), normally present in the seminal fluid. Our results suggest that SP is the molecular switch that promotes wakefulness in the post-mated female, a change of behaviour compatible with increased foraging and egg-laying activity. The stress resulting from SP-dependent sleep deprivation might be an important contribution to the toxic side-effects of male accessory gland products that are known to reduce lifespan in post-mated females.     

High-density interspecific genetic maps of kiwifruit and the identification of sex-specific markers

Kiwifruit (Actinidia chinensis Planchon) is an important specialty fruit crop that suffers from narrow genetic diversity stemming from recent global commercialization and limited cultivar improvement. Here, we present high-density RAD-seq-based genetic maps using an interspecific F₁ cross between Actinidia rufa ‘MT570001’ and A. chinensis ‘Guihai No4’. The A. rufa (maternal) map consists of 2,426 single-nucleotide polymorphism (SNP) markers with a total length of 2,651 cM in 29 linkage groups (LGs) corresponding to the 29 chromosomes. The A. chinensis (paternal) map consists of 4,214 SNP markers over 3,142 cM in 29 LGs. Using these maps, we were able to anchor an additional 440 scaffolds from the kiwifruit draft genome assembly. Kiwifruit is functionally dioecious, which presents unique challenges for breeding and production. Three sex-specific simple sequence repeats (SSR) markers can be used to accurately sex type male and female kiwifruit in breeding programmes. The sex-determination region (SDR) in kiwifruit was narrowed to a 1-Mb subtelomeric region on chromosome 25. Localizing the SDR will expedite the discovery of genes controlling carpel abortion in males and pollen sterility in females.     

Genetic and ‘cultural’ similarity in wild chimpanzees

The question of whether animals possess ‘cultures’ or ‘traditions’ continues to generate widespread theoretical and empirical interest. Studies of wild chimpanzees have featured prominently in this discussion, as the dominant approach used to identify culture in wild animals was first applied to them. This procedure, the ‘method of exclusion,’ begins by documenting behavioural differences between groups and then infers the existence of culture by eliminating ecological explanations for their occurrence. The validity of this approach has been questioned because genetic differences between groups have not explicitly been ruled out as a factor contributing to between-group differences in behaviour. Here we investigate this issue directly by analysing genetic and behavioural data from nine groups of wild chimpanzees. We find that the overall levels of genetic and behavioural dissimilarity between groups are highly and statistically significantly correlated. Additional analyses show that only a very small number of behaviours vary between genetically similar groups, and that there is no obvious pattern as to which classes of behaviours (e.g. tool-use versus communicative) have a distribution that matches patterns of between-group genetic dissimilarity. These results indicate that genetic dissimilarity cannot be eliminated as playing a major role in generating group differences in chimpanzee behaviour.