Sexual selection protects against extinction.

Reproduction through sex carries substantial costs, mainly because only half of sexual adults produce offspring. It has been theorized that these costs could be countered if sex allows sexual selection to clear the universal fitness constraint of mutation load. Under sexual selection, competition between (usually) males and mate choice by (usually) females create important intraspecific filters for reproductive success, so that only a subset of males gains paternity. If reproductive success under sexual selection is dependent on individual condition, which is contingent to mutation load, then sexually selected filtering through 'genic capture' could offset the costs of sex because it provides genetic benefits to populations. Here we test this theory experimentally by comparing whether populations with histories of strong versus weak sexual selection purge mutation load and resist extinction differently. After evolving replicate populations of the flour beetle Tribolium castaneum for 6 to 7 years under conditions that differed solely in the strengths of sexual selection, we revealed mutation load using inbreeding. Lineages from populations that had previously experienced strong sexual selection were resilient to extinction and maintained fitness under inbreeding, with some families continuing to survive after 20 generations of sib × sib mating. By contrast, lineages derived from populations that experienced weak or non-existent sexual selection showed rapid fitness declines under inbreeding, and all were extinct after generation 10. Multiple mutations across the genome with individually small effects can be difficult to clear, yet sum to a significant fitness load; our findings reveal that sexual selection reduces this load, improving population viability in the face of genetic stress.

Mating patterns influence vulnerability to the extinction vortex.

Earth's biodiversity is undergoing mass extinction due to anthropogenic compounding of environmental, demographic and genetic stresses. These different stresses can trap populations within a reinforcing feedback loop known as the extinction vortex, in which synergistic pressures build upon one another through time, driving down population viability. Sexual selection, the widespread evolutionary force arising from competition, choice and reproductive variance within animal mating patterns could have vital consequences for population viability and the extinction vortex: (a) if sexual selection reinforces natural selection to fix 'good genes' and purge 'bad genes', then mating patterns encouraging competition and choice may help protect populations from extinction; (b) by contrast, if mating patterns create load through evolutionary or ecological conflict, then population viability could be further reduced by sexual selection. We test between these opposing theories using replicate populations of the model insect Tribolium castaneum exposed to over 10 years of experimental evolution under monogamous versus polyandrous mating patterns. After a 95-generation history of divergence in sexual selection, we compared fitness and extinction of monogamous versus polyandrous populations through an experimental extinction vortex comprising 15 generations of cycling environmental and genetic stresses. Results showed that lineages from monogamous evolutionary backgrounds, with limited opportunities for sexual selection, showed rapid declines in fitness and complete extinction through the vortex. By contrast, fitness of populations from the history of polyandry, with stronger opportunities for sexual selection, declined slowly, with 60% of populations surviving by the study end. The three vortex stresses of (a) nutritional deprivation, (b) thermal stress and (c) genetic bottlenecking had similar impacts on fitness declines and extinction risk, with an overall sigmoid decline in survival through time. We therefore reveal sexual selection as an important force behind lineages facing extinction threats, identifying the relevance of natural mating patterns for conservation management.

Resistance to natural and synthetic gene drive systems.

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.

Environmental quality alters female costs and benefits of evolving under enforced monogamy.

BACKGROUND: Currently many habitats suffer from quality loss due to environmental change. As a consequence, evolutionary trajectories might shift due to environmental effects and potentially increase extinction risk of resident populations. Nevertheless, environmental variation has rarely been incorporated in studies of sexual selection and sexual conflict, although local environments and individuals' condition undoubtedly influence costs and benefits. Here, we utilise polyandrous and monogamous selection lines of flour beetles, which evolved in presence or absence of sexual selection for 39 generations. We specifically investigated effects of low vs. standard food quality (i.e. stressful vs. benign environments) on reproductive success of cross pairs between beetles from the contrasting female and male selection histories to assess gender effects driving fitness. RESULTS: We found a clear interaction of food quality, male selection history and female selection history. Monogamous females generally performed more poorly than polyandrous counterparts, but reproductive success was shaped by selection history of their mates and environmental quality. When monogamous females were paired with polyandrous males in the standard benign environment, females seemed to incur costs, possibly due to sexual conflict. In contrast, in the novel stressful environment, monogamous females profited from mating with polyandrous males, indicating benefits of sexual selection outweigh costs. CONCLUSIONS: Our findings suggest that costs and benefits of sexually selected adaptations in both sexes can be profoundly altered by environmental quality. With regard to understanding possible impacts of environmental change, our results further show that the ecology of mating systems and associated selection pressures should be considered in greater detail.

No fitness effects of same-sex copulations in male red flour beetles.

Same-sex sexual behavior occurs in diverse animal taxa, yet its evolutionary maintenance is poorly understood as such behavior seems to be costly and does not directly increase reproductive success. We used male Tribolium castaneum beetles, which frequently engage in same-sex copulations, to test if same-sex sexual behavior influences future male mating behavior and reproductive success of males. Furthermore, we tested whether same-sex sexual behavior has benefits via indirect sperm translocation. We conducted a series of mating trials demonstrating that males exposed to same-sex behavior did not sire less offspring compared to control males that did not engage in same-sex behavior. This suggests that same-sex copulations did not lead to fitness costs in subsequent mating interactions. In addition, we found no evidence that indirect sperm translocation via an intermediate male occurs in T. castaneum. Taken together, these results imply that same-sex sexual behavior in males is associated with no costs in terms of lower mating rate and reduced siring success and does not seem to entail benefits. Moreover, our data conform to the hypothesis that sexual indiscrimination is prevalent in this species, which may explain the relatively high frequency of same-sex sexual behavior in T. castaneum.

Coevolving parasites and population size shape the evolution of mating behaviour.

BACKGROUND: Coevolution with parasites and population size are both expected to influence the evolution of mating rates. To gain insights into the interaction between these dual selective factors, we used populations from a coevolution experiment with the red flour beetle, Tribolium castaneum, and its microsporidian parasite, Nosema whitei. We maintained each experimental population at two different population sizes. We assayed the mating behaviour of both males and females from coevolved and paired non-coevolved control populations after 24 generations of coevolution with parasites. RESULTS: Males from large, coevolved populations (i.e. ancestors were exposed to parasites) showed a reduced eagerness to mate compared to males from large, non-coevolved populations. But in small populations, coevolution did not lead to decreased male mating rates. Coevolved females from both large and small populations appeared to be more willing to accept mating than non-coevolved females. CONCLUSIONS: This study provides unique, experimental insights into the combined roles of coevolving parasites and population size on the evolution of mating rate. Furthermore, we find that males and females respond differently to the same environmental conditions. Our results show that parasites can be key determinants of the sexual behaviour of their hosts.

Infections with the microbe Cardinium in the Dolichopodidae and other Empidoidea.

Maternally transmitted reproductive parasites such as Wolbachia and Cardinium can drastically reshape reproduction in their hosts. Beyond skewing sex ratios towards females, these microbes can also cause cytoplasmic incompatibility. Wolbachia probably infects two thirds of insects, but far less is known about the occurrence or action of other bacteria with potentially similar effects. In contrast with the two more widespread reproductive parasites, Wolbachia and Spiroplasma, far less is known of infections with Cardinium (Bacteroidetes) and possible consequences in the Diptera. Here, in an extensive survey, 244 dipteran species from 67 genera belonging to the Dolichopodidae, Empididae, and Hybotidae were assessed for the presence of the microbe Cardinium. Although 130 of the species screened tested positive (ca. 53%), the presence of Cardinium could only be confirmed in 10 species (ca. 4%) based on analysis of sequences. Numerous additional sequences were found to be assignable to known or unknown Bacteroidetes. Considering the known issues concerning specificity of Cardinium primers and the phylogenetic uncertainties surrounding this microbe, the actual prevalence of this symbiont is worthy of further scrutiny. Potential directions for future research on Cardinium-host interactions in Diptera and in general are discussed.

Infection by dsRNA viruses is associated with enhanced sporulation efficiency in Saccharomyces cerevisiae.

Upon starvation diploid cells of the facultative sexual yeast Saccharomyces cerevisiae undergo sporulation, forming four metabolically quiescent and robust haploid spores encased in a degradable ascus. All endosymbionts, whether they provide net benefits or costs, utilize host resources; in yeast, this should induce an earlier onset of sporulation. Here, we tested whether the presence of endosymbiotic dsRNA viruses (M satellite and L-A helper) correspond with higher sporulation rate of their host, S. cerevisiae. We find that S. cerevisiae hosting both the M and L-A viruses (so-called "killer yeasts") have significantly higher sporulation efficiency than those without. We also found that the removal of the M virus did not reduce sporulation frequency, possibly because the L-A virus still utilizes host resources with and without the M virus. Our findings indicate that either virulent resource use by endosymbionts induces sporulation, or that viruses are spread more frequently to sporulating strains. Further exploration is required to distinguish cause from effect.

Reproductive traits: evidence for sexually selected sperm.

Sperm exhibit extraordinary morphological divergence yet precise evolutionary causes often remain elusive. A quantitative genetic study sheds light on the major role postcopulatory sexual selection could play in determining sperm size.

Scent of a killer: How could killer yeast boost its dispersal?

Vector-borne parasites often manipulate hosts to attract uninfected vectors. For example, parasites causing malaria alter host odor to attract mosquitoes. Here, we discuss the ecology and evolution of fruit-colonizing yeast in a tripartite symbiosis-the so-called "killer yeast" system. "Killer yeast" consists of Saccharomyces cerevisiae yeast hosting two double-stranded RNA viruses (M satellite dsRNAs, L-A dsRNA helper virus). When both dsRNA viruses occur in a yeast cell, the yeast converts to lethal toxin­producing "killer yeast" phenotype that kills uninfected yeasts. Yeasts on ephemeral fruits attract insect vectors to colonize new habitats. As the viruses have no extracellular stage, they depend on the same insect vectors as yeast for their dispersal. Viruses also benefit from yeast dispersal as this promotes yeast to reproduce sexually, which is how viruses can transmit to uninfected yeast strains. We tested whether insect vectors are more attracted to killer yeasts than to non­killer yeasts. In our field experiment, we found that killer yeasts were more attractive to Drosophila than non-killer yeasts. This suggests that vectors foraging on yeast are more likely to transmit yeast with a killer phenotype, allowing the viruses to colonize those uninfected yeast strains that engage in sexual reproduction with the killer yeast. Beyond insights into the basic ecology of the killer yeast system, our results suggest that viruses could increase transmission success by manipulating the insect vectors of their host.

Evolutionary conflicts: rapid suppression of a male-killer.

Conflicts between and within species can drive fast evolutionary change. A recent study has documented remarkably rapid counter-adaptations in the wild to an extreme sex-ratio distortion caused by a bacterial symbiont.

Inbreeding depresses sperm competitiveness, but not fertilization or mating success in male Tribolium castaneum.

As populations decline to levels where reproduction among close genetic relatives becomes more probable, subsequent increases in homozygous recessive deleterious expression and/or loss of heterozygote advantage can lead to inbreeding depression. Here, we measure how inbreeding across replicate lines of the flour beetle Tribolium castaneum impacts on male reproductive fitness in the absence or presence of male-male competition. Effects on male evolution from mating pattern were removed by enforcing monogamous mating throughout. After inbreeding across eight generations, we found that male fertility in the absence of competition was unaffected. However, we found significant inbreeding depression of sperm competitiveness: non-inbred males won 57 per cent of fertilizations in competition, while inbred equivalents only sired 42 per cent. We also found that the P(2) 'offence' role in sperm competition was significantly more depressed under inbreeding than sperm 'defence' (P(1)). Mating behaviour did not explain these differences, and there was no difference in the viability of offspring sired by inbred or non-inbred males. Sperm length variation was significantly greater in the ejaculates of inbred males. Our results show that male ability to achieve normal fertilization success was not depressed under strong inbreeding, but that inbreeding depression in these traits occurred when conditions of sperm competition were generated.

The evolution of reproductive isolation through sexual conflict.

Classical population-genetics theory suggests that reproductive isolation will evolve fastest in small isolated populations. In contrast, recent theory suggests that divergence should occur fastest in larger allopatric populations. The rationale behind this is that sexual conflict, potentially the strongest driver of speciation, is greater in larger, higher-density populations. This idea is highly controversial and has little experimental support. Here we show, using replicate fly populations with varying levels of sexual conflict, that larger, more dense populations with more sexual conflict diverged to a greater degree than small populations with relaxed conflict. This result strongly suggests that speciation can occur rapidly in large populations through increased sexual conflict.

Microbial modification of host long-distance dispersal capacity.

BACKGROUND: Dispersal plays a key role in shaping biological and ecological processes such as the distribution of spatially-structured populations or the pace and scale of invasion. Here we have studied the relationship between long-distance dispersal behaviour of a pest-controlling money spider, Erigone atra, and the distribution of maternally acquired endosymbionts within the wider meta-population. This spider persists in heterogeneous environments because of its ability to recolonise areas through active long-distance airborne dispersal using silk as a sail, in a process termed 'ballooning'. RESULTS: We show that there is spatial heterogeneity in the prevalence of two maternally acquired endosymbiont infections within the wider E. atra meta-population and we demonstrate through several independent approaches a link between the presence of one of these endosymbionts, Rickettsia, and the tendency for long-distance movement. CONCLUSION: This novel finding that particular endosymbionts can influence host dispersal is of broad importance given the extremely widespread occurrence of similar bacteria within arthropod communities. A bacterial phenotype that limits dispersal has the potential not only to reduce gene flow and thus contribute to degrees of reproductive isolation within species, but also to influence species distribution and thus overall community composition.

The karyotype of the yellow dung fly, Scathophaga stercoraria, a model organism in studies of sexual selection.

Knowledge of karyotypical characteristics of a species is essential for understanding how sexually selected and sexually antagonistic traits evolve. The yellow dung fly Scathophaga stercoraria L. (Diptera: Scathophagidae) is an established model system for studies of sexual selection and sexual conflict, but karyotypical data are lacking to date. Here, the karyotype of S. stercoraria was characterized using conventional Giemsa-staining and C-banding techniques. The diploid chromosome set consists of 6 pairs of bi-armed meta- or submetacentric chromosomes. The sex chromosomes are the largest chromosomes and constitute 30% of the total length of the diploid set in females and about 25% in males. Males are the heterogametic sex, and the length of the Y chromosome is about three-quarters of that of the X chromosome. C-banding revealed that both sex chromosomes are largely heterochromatic. In contrast, in the five autosome pairs, heterochromatin is limited to narrow bands in the centromeric regions. This karyotypic information will help provide a more profound understanding of the inheritance of phenotypic variation in reproductive traits and the chromosomal locations of underlying genes.

Longevity and developmental stability in the dung fly Sepsis cynipsea, as affected by the ectoparasitic mite, Pediculoides mesembrinae.

Fluctuating asymmetry (FA) is a widely employed measure of developmental stability. It has been found to increase with many stressors including parasite infection. Associations between parasites and FA may exist for several reasons in addition to parasites being the direct cause of increased FA. Developmentally stable individuals may have superior immune systems, and be less susceptible to parasite infection, and/or may be less exposed to parasites than developmentally unstable ones. Mites negatively impact host fitness in a number of insects, and if FA is a reflection of general genetic quality, as has been proposed, associations between mite number and FA are predicted. Potential relationships were investigated between an ectoparasitic mite, Pediculoides mesembrinae (Canestrini) (Phthiraptera: Menoponidae) and FA in the common dung fly Sepsis cynipsea (L.) (Diptera: Sepsidae). While it was found that mite infested flies died much faster than flies without mites, indicating that mites indeed stress their hosts, counter to expectations, no associations between mites and FA were found in any analyses. Additionally, FA in mite-infected flies generally did not differ from previously published FA data from uninfected S. cynipsea. Nevertheless, parasitized males tended to be somewhat less asymmetrical than non-parasitized males, but based on our data, it does not appear that mite infestation is generally associated with developmental stability in S. cynipsea.

Phylogenetics of the Spiroplasma ixodetis endosymbiont reveals past transfers between ticks and other arthropods.

The bacterium Spiroplasma ixodetis is a maternally inherited endosymbiont primarily described from ticks but also found widespread across other arthropods. While it has been identified as a male-killing agent in some insect species, the consequences of infection with S. ixodetis in ticks are entirely unknown, and it is unclear how this endosymbiont spreads across tick species. Here, we have investigated this aspect through the examination of the diversity and evolutionary history of S. ixodetis infections in 12 tick species and 12 other arthropod species. Using a multi-locus typing approach, we identified that ticks harbor a substantial diversity of divergent S. ixodetis strains. Phylogenetic investigations revealed that these S. ixodetis strains do not cluster within a tick-specific subclade but rather exhibit distinct evolutionary origins. In their past, these strains have undergone repeated horizontal transfers between ticks and other arthropods, including aphids and flies. This diversity pattern strongly suggests that maternal inheritance and horizontal transfers are key drivers of S. ixodetis spread, dictating global incidence of infections across tick communities. We do not, however, detect evidence of S. ixodetis-based male-killing since we observed that infections were widely present in both males and females across populations of the African blue tick Rhipicephalus decoloratus.

Lineages evolved under stronger sexual selection show superior ability to invade conspecific competitor populations.

Despite limitations on offspring production, almost all multicellular species use sex to reproduce. Sex gives rise to sexual selection, a widespread force operating through competition and choice within reproduction, however, it remains unclear whether sexual selection is beneficial for total lineage fitness, or if it acts as a constraint. Sexual selection could be a positive force because of selection on improved individual condition and purging of mutation load, summing into lineages with superior fitness. On the other hand, sexual selection could negate potential net fitness through the actions of sexual conflict, or because of tensions between investment in sexually selected and naturally selected traits. Here, we explore these ideas using a multigenerational invasion challenge to measure consequences of sexual selection for the overall net fitness of a lineage. After applying experimental evolution under strong versus weak regimes of sexual selection for 77 generations with the flour beetle Tribolium castaneum, we measured the overall ability of introductions from either regime to invade into conspecific competitor populations across eight generations. Results showed that populations from stronger sexual selection backgrounds had superior net fitness, invading more rapidly and completely than counterparts from weak sexual selection backgrounds. Despite comprising only 10% of each population at the start of the invasion experiment, colonizations from strong sexual selection histories eventually achieved near-total introgression, almost completely eliminating the original competitor genotype. Population genetic simulations using the design and parameters of our experiment indicate that this invasion superiority could be explained if strong sexual selection had improved both juvenile and adult fitness, in both sexes. Using a combination of empirical and modeling approaches, our findings therefore reveal positive and wide-reaching impacts of sexual selection for net population fitness when facing the broad challenge of invading competitor populations across multiple generations.

Reproductive consequences of population divergence through sexual conflict.

Sexual-selection research increasingly focuses on reproductive conflicts between the sexes. Sexual conflict, divergent evolutionary interests of males and females, can cause rapid antagonistic coevolution of reproductive traits and is a potentially powerful speciation engine. This idea has theoretical and comparative support but remains controversial. Recent experimental evidence from Sepsis cynipsea indicates that populations with greater sexual conflict diverged more quickly; females were less likely to mate with males from other populations when flies had evolved under high levels of sexual conflict. The consequences of this divergence have not been addressed, so here we assess two female fitness surrogates after 44 generations of evolving (and diverging) under three different levels of sexual conflict. Longevity after copulation was negatively associated with the degree of sexual conflict under which flies evolved, and housing females with males also reduced female longevity. Female lifetime reproductive success (LRS) also tended to decrease with increasing conflict. However, there was evidence of either sexual-selection fitness benefits at intermediate levels of sexual selection and conflict or inbreeding depression in the smallest populations (those with the lowest levels of conflict). Nevertheless, the results indicate that there can be a fitness load associated with sexual selection and support claims that sexual conflict can lead to reproductive isolation.

Lack of support for Rensch's rule in an intraspecific test using red flour beetle (Tribolium castaneum) populations.

Rensch's rule proposes a universal allometric scaling phenomenon across species where sexual size dimorphism (SSD) has evolved: in taxa with male-biased dimorphism, degree of SSD should increase with overall body size, and in taxa with female-biased dimorphism, degree of SSD should decrease with increasing average body size. Rensch's rule appears to hold widely across taxa where SSD is male-biased, but not consistently when SSD is female-biased. Furthermore, studies addressing this question within species are rare, so it remains unclear whether this rule applies at the intraspecific level. We assess body size and SSD within Tribolium castaneum (Herbst), a species where females are larger than males, using 21 populations derived from separate locations across the world, and maintained in isolated laboratory culture for at least 20 years. Body size, and hence SSD patterns, are highly susceptible to variations in temperature, diet quality and other environmental factors. Crucially, here we nullify interference of such confounds as all populations were maintained under identical conditions (similar densities, standard diet and exposed to identical temperature, relative humidity and photoperiod). We measured thirty beetles of each sex for all populations, and found body size variation across populations, and (as expected) female-biased SSD in all populations. We test whether Rensch's rule holds for our populations, but find isometry, i.e. no allometry for SSD. Our results thus show that Rensch's rule does not hold across populations within this species. Our intraspecific test matches previous interspecific studies showing that Rensch's rule fails in species with female-biased SSD.