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Selfish genetic elements (SGEs), specifically X-chromosome meiotic drive (XCMD), create huge conflicts within a host’s genome and can have profound effects on fertility. Suppressors are a common evolutionary response to XCMD to negate its costs. However, whether suppressors themselves can cause negative non-target effects remains understudied. Here, we examine whether the intragenomic conflicts created by XCMD and its suppressor affects gonad morphology inDrosophila subobscura. We found significant differences in testes, seminal vesicle, and accessory gland size depending on whether a male carried a non-driving X chromosome, an XCMD, and if the XCMD was suppressed. We also found the first evidence of extreme whole-organ damage to testes that is specifically associated with a suppressor of XCMD. Unlike other studies, our evidence suggests that XCMD inD. subobscurainflicts extreme damage on male gonads. This damage is most severe if both XCMD and its suppressor are both present. While costs of suppression have importance in theoretical models, they have largely been ignored in empirical XCMD systems. Overall, this study highlights that genetic conflict, created by SGEs and their suppressors, is a potent evolutionary force that can have major impacts on gonad development and gametogenesis.

Many arthropod species are vulnerable to infection by bacteria that kill the male offspring of their female hosts. These male-killing bacteria (MKB) can greatly impact the ecology and evolution of their hosts, particularly when MKB prevalence is high and persistent through time. However, we still do not have a holistic understanding of the key determinants of MKB ecological epidemiology, particularly regarding the interplay between host-MKB traits and environmental conditions. Here, we derived a mathematical model to analyse the role that several intrinsic and extrinsic factors play in determining MKB epidemiology, and how these factors interact with one another. We found that the invasion threshold and prevalence of MKB is determined by transmission rate and the rate at which female hosts recover from MKB infections. The invasion and prevalence of MKB is also highly sensitive to the extent that MKB can reduce intra-brood competition by killing male offspring. Environmentally-induced periodic changes to the epidemiological characteristics of MKB caused a sharp decline and a slow recovery of MKB prevalence and, in some cases, environmental disturbance can drive MKB extinct. Furthermore, the magnitude of the impact that environmental disturbance had on the dynamics of MKB prevalence was heavily modulated by intrinsic factors, particularly intra-brood competition. This is the first study to explore how both intrinsic and extrinsic factors interact to influence the dynamics of MKB infections over large timescales; our findings are central to predicting the current and future impacts of MKB on host populations.

Attempts to control insect pests and disease vectors have a long history. Recently, new technology has opened a whole new range of possible methods to suppress or transform natural populations. But it has also become clear that a better understanding of the ecology of targeted populations is needed. One key parameter is mating behaviour. Often modified males are released which need to successfully reproduce with females while competing with wild males. Insect control techniques can be affected by target species’ mating ecology, and conversely mating ecology is likely to evolve in response to manipulation attempts. A better understanding of (female) mating behaviour will help anticipate and overcome potential challenges, and thus make desirable outcomes more likely.

Attempts to link physiological thermal tolerance to global species distributions have relied on lethal temperature limits, yet many organisms lose fertility at sublethal temperatures. Here we show that, across 43 Drosophila species, global distributions better match male-sterilizing temperatures than lethal temperatures. This suggests that species distributions may be determined by thermal limits to reproduction, not survival, meaning we may be underestimating the impacts of climate change for many organisms. Prediction of current and future species distributions using thermal limits often relies on lethal temperatures, yet many organisms lose fertility at sublethal temperatures. The authors show that distributions of 43 Drosophila species better match male-sterilizing, than lethal, temperatures.

Few interventions addressing student wellbeing have been designed or evaluated specifically with doctoral students in mind despite the doctoral experience being distinct from that of other students. We therefore explore the benefits of interventions designed specifically to address a key source of stress or anxiety for doctoral students, namely thesis writing. This research uses a mixed-methods approach to explore the ways in which doctoral thesis writing support sessions, in the form of writing workshops or writing retreats, can reduce the stress and anxiety associated with thesis writing specifically or academic writing more generally. Firstly, we quantified the reduction in writing related stress and anxiety associated with workshop participation using a survey completed before and after workshop attendance. Subsequently, we gathered student experiences of workshop participation through focus group interviews. Survey responses showed a clear reduction in participants’ levels of stress and anxiety related to thesis writing and focus group respondents described many clear benefits of participating in writing support sessions. We conclude that participation in thesis writing workshops and writing retreats is a valuable strategy for reducing stress and anxiety associated with thesis writing. The sense of empowerment and confidence that comes from discussing thesis writing in a supportive environment with others in the same situation, and the opportunity to experiment with new tools and strategies, is very valuable for improving the wellbeing of doctoral students.

Selfish genetic elements (SGEs) are diverse and near ubiquitous in Eukaryotes and can be potent drivers of evolution. Here, we discuss SGEs that specifically act on sperm to gain a transmission advantage to the next generation. The diverse SGEs that affect sperm often impose costs on carrier males, including damaging ejaculates, skewing offspring sex ratios and in particular reducing sperm-competitive success of SGE-carrying males. How males and females tolerate and mitigate against these costs is a dynamic and expanding area of research. The intense intra-genomic conflict that these selfish elements generate could also have implications for male fertility and spermatogenesis more widely.This article is part of the theme issue ‘Fifty years of sperm competition’.

Scientists are rapidly developing synthetic gene drive elements intended for release into natural populations. These are intended to control or eradicate disease vectors and pests, or to spread useful traits through wild populations for disease control or conservation purposes. However, a crucial problem for gene drives is the evolution of resistance against them, preventing their spread. Understanding the mechanisms by which populations might evolve resistance is essential for engineering effective gene drive systems. This review summarizes our current knowledge of drive resistance in both natural and synthetic gene drives. We explore how insights from naturally occurring and synthetic drive systems can be integrated to improve the design of gene drives, better predict the outcome of releases and understand genomic conflict in general., Journal of Evolutionary Biology, 33 (10), ISSN:1010-061X, ISSN:1420-9101

Abstract Distinct behaviours can co-vary within individuals. As such, the magnitude of certain behaviours may be partly predicted by other behaviours, rather than the environment. This can constrain behaviours, potentially reducing behavioural variability. Pre-copulatory sexual cannibalism, the consumption of potential mates before copulation, can lead to females remaining unmated, particularly if males are rare. One possible explanation for the persistence of pre-copulatory cannibalism is that sexual cannibalism is correlated with high levels of aggression towards prey. Here, we test this in two species of praying mantis: the highly cannibalistic Miomantis caffra and the less cannibalistic Orthodera novaezealandiae. If cannibalism in M. caffra is linked to aggression towards prey, we predicted that (1) M. caffra would be more aggressive towards prey than O. novaezealandiae, (2) female M. caffra would be more aggressive than males, (3) aggression towards prey would be correlated across juvenile and adult instars for M. caffra but not O. novaezealandiae, and (4) aggression towards prey would be associated with a propensity for sexual cannibalism among individual M. caffra. We found evidence supporting predictions one and two, but not predictions three and four. Surprisingly, aggression was shown to be repeatable and correlated across instars for O. novaezealandiae but not M. caffra. Our results suggest sexual cannibalism is not a product of behavioural co-variation, even in clades where sexual cannibalism is common. This suggests that sexual cannibalism evolves due to the direct benefits it brings to females, rather than being a by-product of high aggression towards heterospecific prey. Significance statement In some animals, different behaviours co-vary within individuals. This may lead to the emergence of costly behaviours and reduce behavioural plasticity. It is theorized that pre-copulatory cannibalism is a costly behavioural by-product of selection for high levels of aggression towards prey. However, there are very few studies that explicitly test this. Here, we provide a behavioural comparison between two species of praying mantis that vary in their propensity to cannibalize and tested whether general aggression is linked cannibalism. We found that aggression towards prey in adults can be linked to juvenile aggression but not a propensity for cannibalism. Although cannibalism rates were higher in the species that was more aggressive towards prey, aggression towards prey was not linked to cannibalism within individuals. This suggests that pre-copulatory cannibalism is not a behavioural by-product but a result of direct selection.

Identifying loci associated with a phenotype is a critical step in many evolutionary studies. Most methods require large sample sizes or breeding designs that can be prohibitively difficult. Here we apply a rarely used approach to identify SNP loci associated with a complex phenotype. We mate siblings from isofemale lines isolate genotypes from three wild populations. After phenotyping we perform whole genome sequencing of isofemale lines from the extremes of the phenotypic distribution of each population and identify SNPs that are consistently fixed for alternative alleles across line pairs. The focal phenotype is female remating rate in the fly Drosophila pseudoobscura, defined as the willingness of a female to mate with a second male after her first mating. This is an integral part of mating system evolution, sexual selection and sexual conflict, and is a quantitative polygenic trait.About 200 SNPs are consistently fixed for alternate alleles in the three pairs of isofemale lines. We use different simulation approaches to explore how many SNPs would be expected to be fixed. We find the surprising result that we uncover fewer observed fixed SNPs than are expected by either simulation approach. We also complete functional analyses of these SNPs. Many lie near genes or regulatory regions known to be involved in Drosophila courtship and mating behaviours, and some have previously been associated with re-mating rates in Genome-Wide Association Studies. Given the small sample size, these results should be treated with caution. Nevertheless, this study suggests that even from a relatively small number of isofemale lines established from wild populations, it is possible to identify candidate loci potentially associated with a complex quantitative trait. However, further work is required to understand modelling the expected distribution of differences.

Predicting how biodiversity will respond to increased temperatures caused by climate change is vital. However, our understanding of the traits that determine species’ response to thermal stress remains incomplete. Laboratory measurements of lethal temperatures have successfully been used to predict global species distributions and the vulnerability of species to future climate change. However, although it has long been known that fertility is sensitive to heat stress, temperatures that cause sterility have not been incorporated into predictions about how climate change will affect biodiversity. Here we show that male sterility temperatures predict the global distributions of 43 species of Drosophila substantially better than their lethal temperatures. This strongly suggests that thermal limits to reproduction can underpin how temperature affects species’ distributions. High temperatures impair male fertility across a broad range of animals and plants, so many organisms may be more vulnerable to high temperatures than currently expected.

Gene drive is a naturally occurring phenomenon in which selfish genetic elements manipulate gametogenesis and reproduction to increase their own transmission to the next generation. Currently, there is great excitement about the potential of harnessing such systems to control major pest and vector populations. If synthetic gene drive systems can be constructed and applied to key species, they may be able to rapidly spread either modifying or eliminating the targeted populations. This approach has been lauded as a revolutionary and efficient mechanism to control insect-borne diseases and crop pests. Driving endosymbionts have already been deployed to combat the transmission of dengue and Zika virus in mosquitoes. However, there are a variety of barriers to successfully implementing gene drive techniques in wild populations. There is a risk that targeted organisms will rapidly evolve an ability to suppress the synthetic drive system, rendering it ineffective. There are also potential risks of synthetic gene drivers invading non-target species or populations. This Special Feature covers the current state of affairs regarding both natural and synthetic gene drive systems with the aim to identify knowledge gaps. By understanding how natural drive systems spread through populations, we may be able to better predict the outcomes of synthetic drive release.

Infertility is common in nature despite its obvious cost to individual fitness. Rising global temperatures are predicted to decrease fertility, and male sterility is frequently used in attempts to regulate pest or disease vector populations. When males are infertile, females may mate with multiple males to ensure fertilization, and changes in female mating behavior in turn could intensify selection on male fertility. Fertility assurance is a potentially wide-spread explanation for polyandry, but whether and how it actually contributes to the evolution of polyandry is not clear. Moreover, whether a drop in male fertility would lead to a genetic increase in polyandry depends on whether females respond genetically or through behavioral plasticity to male infertility. Here, we experimentally manipulate male fertility through heat-exposure in Drosophila pseudoobscura, and test female discrimination against infertile males before and after mating. Using isogenic lines, we compare the roles of behaviorally plastic versus genetically fixed polyandry. We find that heat-exposed males are less active and attractive, and that females are more likely to remate after mating with these males. Remating rate increases with reduced reproductive output, indicating that females use current sperm storage threshold to make dynamic remating decisions. After remating with fertile males, females restore normal fecundity levels. Our results suggest that male infertility could explain the evolution of adaptively flexible polyandry, but is less likely to cause an increase in genetic polyandry.

House mice are a major ecosystem pest, particularly threatening island ecosystems as a non-native invasive species. Rapid advances in synthetic biology offer new avenues to control pest species for biodiversity conservation. Recently, a synthetic sperm-killing gene drive construct called t-Sry has been proposed as a means to eradicate target mouse populations owing to a lack of females. A factor that has received little attention in the discussion surrounding such drive applications is polyandry. Previous research has demonstrated that sperm-killing drivers are extremely damaging to a male’s sperm competitive ability. Here, we examine the importance of this effect on the t-Sry system using a theoretical model. We find that polyandry substantially hampers the spread of t-Sry such that release efforts have to be increased three- to sixfold for successful eradication. We discuss the implications of our finding for potential pest control programmes, the risk of drive spread beyond the target population, and the emergence of drive resistance. Our work highlights that a solid understanding of the forces that determine drive dynamics in a natural setting is key for successful drive application, and that exploring the natural diversity of gene drives may inform effective gene drive design.

What drives mating system variation is a major question in evolutionary biology. Female multiple mating (polyandry) has diverse evolutionary consequences, and there are many potential benefits and costs of polyandry. However, our understanding of its evolution is biased towards studies enforcing monandry in polyandrous species. What drives and maintains variation in polyandry between individuals, genotypes, populations and species remains poorly understood. Genetic variation in polyandry may be actively maintained by selection, or arise by chance if polyandry is selectively neutral. In Drosophila pseudoobscura, there is genetic variation in polyandry between and within populations. We used isofemale lines to found replicate populations with high or low initial levels of polyandry and tracked polyandry under experimental evolution over seven generations. Polyandry remained relatively stable, reflecting the starting frequencies of the experimental populations. There were no clear fitness differences between high versus low polyandry genotypes, and there was no signature of balancing selection. We confirmed these patterns in direct comparisons between evolved and ancestral females and found no consequences of polyandry for female fecundity. The absence of differential selection even when initiating populations with major differences in polyandry casts some doubt on the importance of polyandry for female fitness.

Rising global temperatures are threatening biodiversity. Studies on the impact of temperature on natural populations usually use lethal or viability thresholds, termed the 'critical thermal limit' (CTL). However, this overlooks important sublethal impacts of temperature that could affect species' persistence. Here we discuss a critical but overlooked trait: fertility, which can deteriorate at temperatures less severe than an organism's lethal limit. We argue that studies examining the ecological and evolutionary impacts of climate change should consider the 'thermal fertility limit' (TFL) of species; we propose that a framework for the design of TFL studies across taxa be developed. Given the importance of fertility for population persistence, understanding how climate change affects TFLs is vital for the assessment of future biodiversity impacts.

The traditional view of the genome was once that it is broadly cooperative, with all genes working together amicably to improve the success of the individual as a whole. Benefits to the individual, after all, benefit all the component genes, as fair Mendelian inheritance ensures that all the genes and alleles a parent carries are equally likely to be inherited by an offspring. However, more detailed studies of inheritance have shown that this rosy view of cooperation within the genome is untrue. Instead, many genes act selfishly, manipulating gametogenesis to bias transmission in their favor (Burt and Trivers 2006). This increases their representation in offspring at a cost to the fitness of the individual and the cooperative genes. The existence of such selfish genetic elements has revolutionized our view of evolution, showing that cooperation between genetic elements to further the interests of the individual as a whole is not the only way forward (Werren 2011). Indeed, in this special column, Agren (2016) reviews the history of how ideas about selfish genetic elements have interacted with broader evolutionary thought, particularly the contrast between the gene’s eye view of evolution and ideas of multilevel selection. Selfish genetic elements are expected to evolve whenever there is a conflict over transmission—where different genes are transmitted in different ways. For example, nuclear genes are typically inherited through all gametes, whereas genes in organelles are only inherited via eggs, not sperm or pollen, leading to conflicts between organelles and nuclear genes, such as selfish endosymbionts, pollen-killing chloroplasts, and mitonuclear conflict (Burt and Trivers 2006). There is enormous variety in the ways organisms arrange their genomes, package parts of these genomes into gametes, and mix gametes during sex. This diversity means there are likely to be large numbers of undiscovered selfish genes, acting in unexpected ways to …

Females are expected to avoid low-quality males fathering their offspring. X chromosome meiotic drive (XCMD) makes males very low-quality mates. XCMDs are X chromosomes that, in males, cause the failure of all Y chromosome sperm, so all functional sperm carry the driving X and produce daughters. This transmission advantage can allow the XCMD to spread through populations. However, XCMD males typically have low fertility, are very poor at sperm competition, only produce daughters, and bear low fitness alleles associated with XCMD. This imposes significant costs on females that mate with these males. Recently, several studies have shown that females can reduce the risk of their offspring inheriting XCMDs by mating with multiple males (polyandry), as XCMD males typically lose out to normal males in sperm competition. Hence it has been suggested that increased polyandry may be likely to evolve whenever a costly XCMD is common in a population, and that polyandry may be a key factor in preventing XCMDs spreading through populations. We tested this by examining the fruit fly Drosophila subobscura, in which females are known to mate only once in European populations where XCMDs are absent. However, in North African populations an XCMD, referred to as ‘SRs’, occurs. If the association between XCMDs and polyandry is true, then these North African populations should have evolved polyandry. However, we found no evidence of polyandry in North African D. subobscura populations. Instead, we found some evidence that males that carry SRs are slightly less successful at gaining matings in noncompetitive situations. These results show that polyandry does not necessarily evolve in response to the presence of harmful X chromosome drive. With both sperm competition and female choice both being unlikely to substantially reduce the success of XCMD in D. subobscura, the factors that prevent SRs spreading through these populations remain mysterious.

International audience; The microbiota is increasingly being recognized as having important impacts on many host biological processes. However, evidence of its effects on animal communication and breeding strategy is lacking. In this three-factorial study, we show that females were more willing to mate with related males, with relatedness likely being assessed through the microbiota. By contrast, male mating investment is concurrently determined by both the relatedness and microbiota status of the female. When the microbiota in female Drosophila melanogaster is altered by an antibiotic, male investment in sperm number increased when mating with unrelated females compared to related ones. Contrastingly, the presence of an intact microbiota in females canceled this male outbreeding strategy. As a consequence, the microbiota, when intact, decreased the fitness of the mating couple. Furthermore, we showed that female sexual signaling (cuticular hydrocarbons), with regards to kin recognition, significantly interacts with microbiota. Interestingly, the interaction is significant for hydrocarbons expressed by both sexes, but not for female-specific compounds. Taken together, our results suggest that microbiota can influence kin recognition by disfavoring male outbreeding strategies, likely by inhibiting key olfactory sexual signaling. This represents the first evidence of a host outbreeding strategy counteracted by their microbiota. © 2018 Heys, Lizé, Colinet, Price, Prescott, Ingleby and Lewis.

Choosing the right mate can be critical to fitness, particularly for females of species that mate only once. One key trait by which females choose mates is male age. However, while some theories predict that females should prefer older males, others predict exactly the opposite. The evidence is also mixed, with females preferring older males in some species, and younger in others. Here we examined female preference for male age in a monandrous species, the fruit fly Drosophila subobscura. We found consistent preference for older males in four populations, from the U.K., Greece, Spain and Tunisia. Preference for older males was weaker in trials in which two males were presented to a female than in single-male trials. This preference for older males is probably driven by direct benefits: females that mated with older males produced more offspring. As this species is monandrous, it is very likely that this increase in offspring production is a genuine male-derived benefit, rather than females laying more eggs after mating with a preferred male. Previous work suggests that male–male interactions prior to mating can have a major impact on mating behaviour and success in males of this species and other Drosophila. We found varying effects of prior exposure to rival males, but in general younger males suffered more when exposed to a rival than older males. This study suggests that age-based preference by females can be consistent across populations with very different environments, even when those populations differ in other key mating-related traits such as offspring production and copulation duration.

Segregation distorters located on sex chromosomes are predicted to sweep to fixation and cause extinction via a shortage of one sex, but in nature they are often found at low, stable frequencies. One potential resolution to this longstanding puzzle involves female multiple mating (polyandry). Because many meiotic drivers severely reduce the sperm competitive ability of their male carriers, females are predicted to evolve more frequent polyandry and thereby promote sperm competition when a meiotic driver invades. Consequently, the driving chromosome's relative fitness should decline, halting or reversing its spread. We used formal modeling to show that this initially appealing hypothesis cannot resolve the puzzle alone: other selective pressures (e.g., low fitness of drive homozygotes) are required to establish a stable meiotic drive polymorphism. However, polyandry and meiotic drive can strongly affect one another's frequency, and polyandrous populations may be resistant to the invasion of rare drive mutants.

Maternally inherited symbionts are common in arthropods and many have important roles in host adaptation. The observation that specific symbiont lineages infect distantly related host species implies new interactions are commonly established by lateral transfer events. However, studies have shown that symbionts often perform poorly in novel hosts. We hypothesized selection on the symbiont may be sufficiently rapid that poor performance in a novel host environment is rapidly ameliorated, permitting symbiont maintenance. Here, we test this prediction for a Spiroplasma strain transinfected into the novel host Drosophila melanogaster. In the generations immediately following transinfection, the symbiont had low transmission efficiency to offspring and imposed severe fitness costs on its host. We observed that effects on host fitness evolved rapidly, being undetectable after 17 generations in the novel host, whereas vertical transmission efficiency was poorly responsive over this period. Our results suggest that long-term symbiosis may more readily be established in cases where symbionts perform poorly in just one aspect of symbiosis.

Some behaviours that typically increase fitness at the individual level may reduce population persistence, particularly in the face of environmental changes. Sexual cannibalism is an extreme mating behaviour which typically involves a male being devoured by the female immediately before, during or after copulation, and is widespread amongst predatory invertebrates. Although the individual‐level effects of sexual cannibalism are reasonably well understood, very little is known about the population‐level effects. We constructed both a mathematical model and an individual‐based model to predict how sexual cannibalism might affect population growth rate and extinction risk. We found that in the absence of any cannibalism‐derived fecundity benefit, sexual cannibalism is always detrimental to population growth rate and leads to a higher population extinction risk. Increasing the fecundity benefits of sexual cannibalism leads to a consistently higher population growth rate and likely a lower extinction risk. However, even if cannibalism‐derived fecundity benefits are large, very high rates of sexual cannibalism (>70%) can still drive the population to negative growth and potential extinction. Pre‐copulatory cannibalism was particularly damaging for population growth rates and was the main predictor of growth declining below the replacement rate. Surprisingly, post‐copulatory cannibalism had a largely positive effect on population growth rate when fecundity benefits were present. This study is the first to formally estimate the population‐level effects of sexual cannibalism. We highlight the detrimental effect sexual cannibalism may have on population viability if (1) cannibalism rates become high, and/or (2) cannibalism‐derived fecundity benefits become low. Decreased food availability could plausibly both increase the frequency of cannibalism, and reduce the fecundity benefit of cannibalism, suggesting that sexual cannibalism may increase the risk of population collapse in the face of environmental change.

Female multiple mating, known as polyandry, is ubiquitous and occurs in a wide variety of taxa. Polyandry varies greatly from species in which females mate with one or two males in their lifetime to species in which females may mate with several different males on the same day. As multiple mating by females is associated with costs, numerous hypotheses attempt to explain this phenomenon. One hypothesis not extensively explored is the possibility that polyandrous behavior is captured and "fixed" in populations via genetic processes that preserve the behavior independently of any adaptive benefit of polyandry. Here, we use female isolines derived from populations of Drosophila pseudoobscura from three locations in North America to examine whether different female remating levels are associated with patterns of chromosome inversions, which may explain patterns of polyandry across the geographic range. Populations differed with respect to the frequency of polyandry and the presence of inversion polymorphisms on the third chromosome. The population with the lowest level of female remating was the only one that was entirely comprised of homokaryotypic lines, but the small number of populations prevented us investigating this relationship further at a population level. However, we found no strong relationship between female remating levels and specific karyotypes of the various isolines.

Selfish genetic elements such as selfish chromosomes increase their transmission rate relative to the rest of the genome and can generate substantial cost to the organisms that carry them. Such segregation distorters are predicted to either reach fixation (potentially causing population extinction) or, more commonly, promote the evolution of genetic suppression to restore transmission to equality. Many populations show rapid spread of segregation distorters, followed by the rapid evolution of suppression. However, not all drivers display such flux, some instead persisting at stable frequencies in natural populations for decades, perhaps hundreds of thousands of years, with no sign of suppression evolving or the driver spreading to fixation. This represents a major evolutionary paradox. How can drivers be maintained in the long term at stable frequencies? And why has suppression not evolved as in many other gene drive systems? Here, we explore potential factors that may explain the persistence of drive systems, focusing on the ancient sex-ratio driver in the flyDrosophila pseudoobscura. We discuss potential solutions to the evolutionary mystery of why suppression does not appear to have evolved in this system, and address how long-term stable frequencies of gene drive can be maintained. Finally, we speculate whether ancient drivers may be functionally and evolutionarily distinct to young drive systems.

Sexual cannibalism is common in spiders and can be advantageous for female fitness by increasing egg production. However, it is possible that, under low mate density, females will be at risk of consuming all of the males they encounter prior to copulation. Cannibalistic females may be able to mitigate the risk of virgin death if they reduce cannibalism rates in response to low mate availability. Here, we attempted to manipulate perceived mate density and observe whether it affected female aggression towards males in the fen raft spider (Dolomedes fimbriatus). We predicted that female attack rate would increase in response to an increasing number of male encounters. We also recorded male courtship effort. Despite previous literature finding that D. fimbriatus females were highly aggressive towards conspecific males, we found that females only attacked courting males in 14% of encounters. None of these attacks resulted in cannibalism. Moreover, attacks were not associated with how many males the female had previously been exposed to. Male courtship effort decreased in response to repeated exposure to females. Some of the virgin females laid and guarded unfertilized egg cases; this made them unattractive to males, potentially reducing their reproductive lifespan prematurely.

Selfish ‘meiotic drive’ alleles are transmitted to more than 50% of offspring, allowing them to rapidly invade populations even if they reduce the fitness of individuals carrying them. Theory predicts that drivers should either fix or go extinct, yet some drivers defy these predictions by persisting at low, stable frequencies for decades. One possible explanation for this discrepancy is that drivers are especially costly when homozygous, although empirical tests of this idea are rare and equivocal. Here, we measure the fitness of femaleDrosophila pseudoobscuracarrying zero, one or two copies of the X-linked driver sex ratio(SR).SRhad strong negative effects on female offspring production and the probability of reproductive failure, and these effects were largely similar across four genetic backgrounds.SRwas especially costly when homozygous. We used our fitness measurements to parametrize a population genetic model, and found that the female fitness costs observed here can explain the puzzlingly low allele frequency ofSRin nature. We also use the model to show how spatial variation in female mating behaviour, fitness costs ofSRand the reduced siring success ofSRmales can jointly explain the north–south cline inSRfrequencies across North America.

International audience; Males in many taxa exhibit behavioural plasticity in response to the perceived threat of sperm competition. Drosophila males prolong mating in response to the presence of competitor males before copulation. The benefits of this behaviour to males are evident in Drosophila melanogaster. However, the adaptive nature of the trait is challenged by the observation that it is present in four other Drosophila species, two of which are largely monandrous, raising the possibility that this plasticity is not evolutionarily labile. In the present study, behavioural plasticity and the mating system in Drosophila bifasciata Pominini (Diptera, Drosophilidae) are analyzed. By contrast to other Drosophila species, male D. bifasciata do not exhibit plasticity in copulation duration when competitor males are present before mating. Thus, plasticity in mating duration is not fixed in the genus Drosophila. The mating system of D. bifasciata is also examined. The species is polyandrous but, uncommonly for the genus Drosophila, males transfer a mating plug composed of sperm to females, which forms very shortly after copulation and fills the female uterus. The absence of plasticity observed in D. bifasciata may arise from the sperm plug.

Summary1. Selfish genetic elements (SGEs) are universal and can have major evolutionary and ecologicalimpacts, but their ecology is not well understood. Most SGEs have stable population dynamics,but the reasons for this are rarely known. Several SGEs are distributed along latitudinal fre-quency clines, providing an opportunity to examine why these clines are stable.2. Latitudinal temperature changes are a strong contender for an underlying environmentalcause of such clines. Both SGEs and extreme temperatures commonly affect male fertility. Ifthese factors interact to reduce male fertility, this could be the cause of the observed latitudinalclines.3. The meiotic driving X-chromosome sex ratio (SR), found in the fruit fly Drosophila pseud-oobscura, is distributed in a cline across North America, being absent in Canada and increasingin frequency southward to 30% at the Mexico⁄USA border. This cline has been stable for atleast 50 years, despite considerable gene flow between populations. If SR males have decreasedfertility in the colder Northern populations, this could undermine the success of SR and causethis cline.4. Here, we examine the fertility of males reared at high and low temperatures. We find thatboth SR and non-SR males have reduced fertility at high temperatures. However, SR malesshow disproportionally lower fertility at high temperatures than non-SR males.5. The geographical distribution of SR suggests the opposite should be true; SR males should bemore successful at high temperatures than low ones, as SR is more common in the South, hencethe observed temperature-related fertility differences of males cannot be the cause of the cline inSR in nature.6. This study finds that the reduction in male fertility commonly caused by SGEs is temperaturedependent. However, although these interactions are likely to be important for the ecology ofSGEs, they do not necessarily provide the explanation for the observed latitudinal clines in SR.Key-words: Drosophila pseudoobscura, meiotic drive, fertility, selfish genetic elements, matingrate, ejaculate sizeIntroduction

Selfish genetic elements (SGEs) that spread by manipulating spermatogenesis often have highly deleterious effects on males that carry them. Females that mate with male carriers of SGEs can also suffer significant costs: they receive fewer and poorer-quality sperm, their offspring will inherit the deleterious allele, and the sex ratio of their offspring will be biased towards the more common sex. To counter these costs, females are therefore expected to prefer to mate with males that do not carry sex ratio distorters or other deleterious selfish genetic elements. However, despite the potential costs, there are few examples of female choice against males carrying SGEs. We searched for evidence of a female preference in fruit fly Drosophila pseudoobscura against males carrying a costly meiotic driving X-chromosome Sex Ratio (SR). In a series of five non-competitive mate preference experiments, we find no evidence that females prefer to mate with non-SR males. Our use of five separate experiments, involving more than 800 females, makes it unlikely that this lack of a difference was due to low power or simple chance. We suggest that the lack of female choice against SGE-carrying males may be due to strong selection on SGEs to be indistinguishable from alternative alleles. Furthermore, polyandry, either in direct response to receiving an ejaculate from an SGE-carrying male or carried out indiscriminately when at risk of mating with carriers, may be an alternative response by females to limit the exposure of their offspring to SGEs.

Much of our understanding of female mating behaviour in insects comes from studies performed under controlled laboratory conditions, with Drosophila as the most commonly used model system. Laboratory studies of Drosophila have demonstrated a strong genetic basis to female remating rate. Because behaviour is strongly influenced by the environment, the heritability of remating rate in laboratory cultures does not necessarily reflect variation that is relevant to field conditions. In this study, we investigated the strength of the link between the behaviour of flies in laboratory and field. Wild-caught female Drosophila pseudoobscura that produced broods sired by multiple males had daughters that remated more rapidly in the laboratory. This suggests that laboratory experiments can successfully reflect differences between females’ mating behaviour in nature.

In Drosophila melanogaster, the DDT resistance allele (DDT-R) is beneficial in the presence of DDT. Interestingly, DDT-R also elevates female fitness in the absence of DDT and existed in populations before DDT use. However, DDT-R did not spread regardless of DDT-independent selective advantages in females. We ask whether sexual antagonism could explain why DDT-R did not spread before pesticide use. We tested pre- and post-copulatory male fitness correlates in two genetic backgrounds into which we backcrossed the DDT-R allele. We found costs to DDT-R that depended on the genetic background in which DDT-R was found and documented strong epistasis between genetic background and DDT-R that influenced male size. Although it remains unclear whether DDT-R is generally sexually antagonistic, or whether the fitness costs noted would be sufficient to retard the spread of DDT-R in the absence of DDT, general fitness advantages to DDT-R in the absence of DDT may be unlikely.

SummaryFemales of most animal species are polyandrous, with individual females usually mating with more than one male [1, 2]. However, the ubiquity of polyandry remains enigmatic [3, 4] because of the potentially high costs to females of multiple mating [5, 6]. Current theory to account for the high prevalence of polyandry largely focuses on its benefits to individual females [7, 8]. There are also higher-level explanations for the high incidence of polyandry—polyandrous clades may speciate more rapidly [6]. Here we test the hypothesis that polyandry may also reduce population extinction risk. We demonstrate that mating with multiple males protects populations of the fruit fly Drosophila pseudoobscura against extinction caused by a “selfish” sex-ratio-distorting element. Thus, the frequency of female multiple mating in nature may be associated not only with individual benefits to females of this behavior but also with increased persistence over time of polyandrous species and populations. Furthermore, we show that female remating behavior can determine the frequency of sex-ratio distorters in populations. This may also be true for many other selfish genetic elements in natural populations.

Selfish genetic elements (SGEs) are ubiquitous in animals and often associated with low male fertility due to reduced sperm number in male carriers. In the fruit fly Drosophila pseudoobscura, the meiotic driving X chromosome "sex ratio" kills Y-bearing sperm in carrier males (SR males), resulting in female only broods. We competed SR males against the ejaculates of noncarrying standard males (ST males), and quantified the number of sperm transferred by SR and ST males to females. We show that SR males are very poor sperm competitors, which is partly related to transfer of fewer sperm during mating. However, sperm numbers alone cannot explain the observed paternity reduction, indicating SR males' sperm may be of reduced quality, possibly due to damage during the killing of the noncarrying Y-sperm. The reduction in sperm competitive ability due to SR is large enough to potentially stabilize the spread of sex ratio drive through populations. The poor sperm competitive ability of SR males coupled with their low fitness as mates could favor increased remating by females to reduce paternity by SR males. Given the generally poor performance of SGE-carrying males in sperm competition, this may generate strong selective pressure favoring polyandry in many species.

With respect to mate choice, females of many species discriminate between males on the basis of age. The adaptive significance of age-based mate choice is unclear, with various hypotheses making conflicting predictions. We examined the possibility of female preference in the fruit fly Drosophila pseudoobscura, a species where females gain no significant nutritional benefits from mating. Females were shown to prefer to mate with old males in two-male choice experiments and accepted old males faster than young males in single-male tests. Females mated to old males had a higher fecundity, possibly related to a transfer of more sperm and/or a larger volume of accessory gland proteins during the longer copulation durations experienced with old males, although these possibilities were not directly tested. Hence, females appear to derive direct benefits from preferring to mate with older males. In contrast, there was no evidence of mate preference for the sons of either old or young males when matched for age, indicating that the mating advantage of old males is not passed to their sons. These sets of experiments suggest that in D. pseudoobscura the benefit of age-based preference to females is increased fecundity due to greater investment per mating by older males.

Females of many species mate with more than one male (polyandry), yet the adaptive significance of polyandry is poorly understood. One hypothesis to explain the widespread occurrence of multiple mating is that it may allow females to utilize post-copulatory mechanisms to reduce the risk of fertilizing their eggs with sperm from incompatible males. Selfish genetic elements (SGEs) are ubiquitous in eukaryotes, frequent sources of reproductive incompatibilities, and associated with fitness costs. However, their impact on sexual selection is largely unexplored. In this review we examine the link between SGEs, male fertility and sperm competitive ability. We show there is widespread evidence that SGEs are associated with reduced fertility in both animals and plants, and present some recent data showing that males carrying SGEs have reduced paternity in sperm competition. We also discuss possible reasons why male gametes are particularly vulnerable to the selfish actions of SGEs. The widespread reduction in male fertility caused by SGEs implies polyandry may be a successful female strategy to bias paternity against SGE-carrying males.

Mating experiments using Drosophila have contributed greatly to the understanding of sexual selection and behavior. Experiments often require simple, easy and cheap methods to distinguish between individuals in a trial. A standard technique for this is CO2 anaesthesia and then labelling or wing clipping each fly. However, this is invasive and has been shown to affect behavior. Other techniques have used coloration to identify flies. This article presents a simple and non-invasive method for labelling Drosophila that allows them to be individually identified within experiments, using food coloring. This method is used in trials where two males compete to mate with a female. Dyeing allowed quick and easy identification. There was, however, some difference in the strength of the coloration across the three species tested. Data is presented showing the dye has a lower impact on mating behavior than CO2 in Drosophila melanogaster. The impact of CO2 anaesthesia is shown to depend on the species of Drosophila, with D. pseudoobscura and D. subobscura showing no impact, whereas D. melanogaster males had reduced mating success. The dye method presented is applicable to a wide range of experimental designs.

One aspect of sexual selection that Darwin was completely unaware of was the role of Selfish Genetic Elements (SGEs). SGEs are genes, organelles or microorganisms present within the genome or cell of an organism that spread through populations by subverting normal patterns of inheritance in ways that increase their representation in the next generation. SGEs are ubiquitous in living organisms, have a dramatic ability to manipulate host reproduction, including the frequent reduction in male fertility and sperm competitive ability, yet their impact on sexual selection remains little explored. Here we discuss the pervasiveness and power of SGEs as an agent of sexual selection and show they can have remarkably wide-ranging impacts on male and female reproduction and therefore in shaping mating systems, even when present at low frequencies.

Background Populations of a species often differ in key traits. However, it is rarely known whether these differences are associated with genetic variation and evolved differences between populations, or are instead simply a plastic response to environmental differences experienced by the populations. Here we examine the interplay of plasticity and direct genetic control by investigating temperature-size relationships in populations of Drosophila pseudoobscura from North America. We used 27 isolines from three populations and exposed them to four temperature regimes (16°C, 20°C, 23°C, 26°C) to examine environmental, genetic and genotype-by-environment sources of variance in wing size. Results By far the largest contribution to variation in wing size came from rearing temperature, with the largest flies emerging from the coolest temperatures. However, we also found a genetic signature that was counter to this pattern as flies originating from the northern, cooler population were consistently smaller than conspecifics from more southern, warmer populations when reared under the same laboratory conditions. Conclusions We conclude that local selection on body size appears to be acting counter to the environmental effect of temperature. We find no evidence that local adaptation in phenotypic plasticity can explain this result, and suggest indirect selection on traits closely linked with body size, or patterns of chromosome inversion may instead be driving this relationship. Electronic supplementary material The online version of this article (doi:10.1186/s12862-015-0323-3) contains supplementary material, which is available to authorized users.