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1.  Quantifying Variability of Avian Colours: Are Signalling Traits More Variable? 
PLoS ONE  2008;3(2):e1689.
Background
Increased variability in sexually selected ornaments, a key assumption of evolutionary theory, is thought to be maintained through condition-dependence. Condition-dependent handicap models of sexual selection predict that (a) sexually selected traits show amplified variability compared to equivalent non-sexually selected traits, and since males are usually the sexually selected sex, that (b) males are more variable than females, and (c) sexually dimorphic traits more variable than monomorphic ones. So far these predictions have only been tested for metric traits. Surprisingly, they have not been examined for bright coloration, one of the most prominent sexual traits. This omission stems from computational difficulties: different types of colours are quantified on different scales precluding the use of coefficients of variation.
Methodology/Principal Findings
Based on physiological models of avian colour vision we develop an index to quantify the degree of discriminable colour variation as it can be perceived by conspecifics. A comparison of variability in ornamental and non-ornamental colours in six bird species confirmed (a) that those coloured patches that are sexually selected or act as indicators of quality show increased chromatic variability. However, we found no support for (b) that males generally show higher levels of variability than females, or (c) that sexual dichromatism per se is associated with increased variability.
Conclusions/Significance
We show that it is currently possible to realistically estimate variability of animal colours as perceived by them, something difficult to achieve with other traits. Increased variability of known sexually-selected/quality-indicating colours in the studied species, provides support to the predictions borne from sexual selection theory but the lack of increased overall variability in males or dimorphic colours in general indicates that sexual differences might not always be shaped by similar selective forces.
doi:10.1371/journal.pone.0001689
PMCID: PMC2253496  PMID: 18301766
2.  The Evolutionary Consequences of Disrupted Male Mating Signals: An Agent-Based Modelling Exploration of Endocrine Disrupting Chemicals in the Guppy 
PLoS ONE  2014;9(7):e103100.
Females may select a mate based on signalling traits that are believed to accurately correlate with heritable aspects of male quality. Anthropogenic actions, in particular chemicals released into the environment, are now disrupting the accuracy of mating signals to convey information about male quality. The long-term prediction for disrupted mating signals is most commonly loss of female preference. Yet, this prediction has rarely been tested using quantitative models. We use agent-based models to explore the effects of rapid disruption of mating signals. In our model, a gene determines survival. Males signal their level of genetic quality via a signal trait, which females use to select a mate. We allowed this system of sexual selection to become established, before introducing a disruption between the male signal trait and quality, which was similar in nature to that induced by exogenous chemicals. Finally, we assessed the capacity of the system to recover from this disruption. We found that within a relatively short time frame, disruption of mating signals led to a lasting loss of female preference. Decreases in mean viability at the population-level were also observed, because sexual-selection acting against newly arising deleterious mutations was relaxed. The ability of the population to recover from disrupted mating signals was strongly influenced by the mechanisms that promoted or maintained genetic diversity in traits under sexual selection. Our simple model demonstrates that environmental perturbations to the accuracy of male mating signals can result in a long-term loss of female preference for those signals within a few generations. What is more, the loss of this preference can have knock-on consequences for mean population fitness.
doi:10.1371/journal.pone.0103100
PMCID: PMC4105596  PMID: 25047080
3.  Condition-dependent expression of pre- and postcopulatory sexual traits in guppies 
Ecology and Evolution  2013;3(7):2197-2213.
Female choice can impose persistent directional selection on male sexually selected traits, yet such traits often exhibit high levels of phenotypic variation. One explanation for this paradox is that if sexually selected traits are costly, only the fittest males are able to acquire and allocate the resources required for their expression. Furthermore, because male condition is dependent on resource allocation, condition dependence in sexual traits is expected to underlie trade-offs between reproduction and other life-history functions. In this study we test these ideas by experimentally manipulating diet quality (carotenoid levels) and quantity in the guppy (Poecilia reticulata), a livebearing freshwater fish that is an important model for understanding relationships between pre- and post-copulatory sexually selected traits. Specifically, we test for condition dependence in the expression of pre- and postcopulatory sexual traits (behavior, ornamentation, sperm traits) and determine whether diet manipulation mediates relationships among these traits. Consistent with prior work we found a significant effect of diet quantity on the expression of both pre- and postcopulatory male traits; diet-restricted males performed fewer sexual behaviors and exhibited significant reductions in color ornamentation, sperm quality, sperm number, and sperm length than those fed ad libitum. However, contrary to our expectations, we found no significant effect of carotenoid manipulation on the expression of any of these traits, and no evidence for a trade-off in resource allocation between pre- and postcopulatory episodes of sexual selection. Our results further underscore the sensitivity of behavioral, ornamental, and ejaculate traits to dietary stress, and highlight the important role of condition dependence in maintaining the high variability in male sexual traits.
doi:10.1002/ece3.632
PMCID: PMC3728957  PMID: 23919162
Carotenoids; dietary manipulation; genetic variation; lek paradox; trade-offs
4.  Both male and female identity influence variation in male signalling effort 
Background
Male sexual displays play an important role in sexual selection by affecting reproductive success. However, for such displays to be useful for female mate choice, courtship should vary more among than within individual males. In this regard, a potentially important source of within male variation is adjustment of male courtship effort in response to female traits. Accordingly, we set out to dissect sources of variation in male courtship effort in a fish, the desert goby (Chlamydogobius eremius). We did so by designing an experiment that allowed simultaneous estimation of within and between male variation in courtship, while also assessing the importance of the males and females as sources of courtship variation.
Results
Although males adjusted their courtship depending on the identity of the female (a potentially important source of within-male variation), among-male differences were considerably greater. In addition, male courtship effort towards a pair of females was highly repeatable over a short time frame.
Conclusion
Despite the plasticity in male courtship effort, courtship displays had the potential to reliably convey information about the male to mate-searching females. Our experiment therefore underscores the importance of addressing the different sources contributing to variation in the expression of sexually-selected traits.
doi:10.1186/1471-2148-11-233
PMCID: PMC3163561  PMID: 21827657
5.  Estimation of heritability, evolvability and genetic correlations of two pollen and pistil traits involved in a sexual conflict over timing of stigma receptivity in Collinsia heterophylla (Plantaginaceae) 
Annals of Botany  2012;110(1):91-99.
Background and Aims
Heritable genetic variation is crucial for selection to operate, yet there is a paucity of studies quantifying such variation in interactive male/female sexual traits, especially those of plants. Previous work on the annual plant Collinsia heterophylla, a mixed-mating species, suggests that delayed stigma receptivity is involved in a sexual conflict: pollen from certain donors fertilize ovules earlier than others at the expense of reduced maternal seed set and lower levels of pollen competition.
Methods
Parent–offspring regressions and sib analyses were performed to test for heritable genetic variation and co-variation in male and female interactive traits related to the sexual conflict.
Key Results
Some heritable variation and evolvability were found for the female trait (delayed stigma receptivity in presence of pollen), but no evidence was found for genetic variation in the male trait (ability to fertilize ovules early). The results further indicated a marginally significant correlation between a male's ability to fertilize early and early stigma receptivity in offspring. However, despite potential indirect selection of these traits, antagonistic co-evolution may not occur given the lack of heritability of the male trait.
Conclusions
To our knowledge, this is the first study of a plant or any hermaphrodite that examines patterns of genetic correlation between two interactive sexual traits, and also the first to assess heritabilities of plant traits putatively involved in a sexual conflict. It is concluded that the ability to delay fertilization in presence of pollen can respond to selection, while the pollen trait has lower evolutionary potential.
doi:10.1093/aob/mcs084
PMCID: PMC3380587  PMID: 22645118
Antagonistic trait; co-evolution; Collinsia heterophylla; evolvability; genetic correlation; genetic variation; heritability; mate choice; pollen competition; sexual conflict; stigma receptivity
6.  Sex allocation and investment into pre- and post-copulatory traits in simultaneous hermaphrodites: the role of polyandry and local sperm competition 
Sex allocation theory predicts the optimal allocation to male and female reproduction in sexual organisms. In animals, most work on sex allocation has focused on species with separate sexes and our understanding of simultaneous hermaphrodites is patchier. Recent theory predicts that sex allocation in simultaneous hermaphrodites should strongly be affected by post-copulatory sexual selection, while the role of pre-copulatory sexual selection is much less clear. Here, we review sex allocation and sexual selection theory for simultaneous hermaphrodites, and identify several strong and potentially unwarranted assumptions. We then present a model that treats allocation to sexually selected traits as components of sex allocation and explore patterns of allocation when some of these assumptions are relaxed. For example, when investment into a male sexually selected trait leads to skews in sperm competition, causing local sperm competition, this is expected to lead to a reduced allocation to sperm production. We conclude that understanding the evolution of sex allocation in simultaneous hermaphrodites requires detailed knowledge of the different sexual selection processes and their relative importance. However, little is currently known quantitatively about sexual selection in simultaneous hermaphrodites, about what the underlying traits are, and about what drives and constrains their evolution. Future work should therefore aim at quantifying sexual selection and identifying the underlying traits along the pre- to post-copulatory axis.
doi:10.1098/rstb.2012.0052
PMCID: PMC3576586  PMID: 23339243
cryptic female choice; multiple mating; pre-copulatory sexual selection; post-copulatory sexual selection; sex allocation; sperm competition
7.  Prevalence of Consensual Male–Male Sex and Sexual Violence, and Associations with HIV in South Africa: A Population-Based Cross-Sectional Study 
PLoS Medicine  2013;10(6):e1001472.
Using a method that offered complete privacy to participants, Rachel Jewkes and colleagues conducted a survey among South African men about their lifetime same-sex experiences.
Please see later in the article for the Editors' Summary
Background
In sub-Saharan Africa the population prevalence of men who have sex with men (MSM) is unknown, as is the population prevalence of male-on-male sexual violence, and whether male-on-male sexual violence may relate to HIV risk. This paper describes lifetime prevalence of consensual male–male sexual behavior and male-on-male sexual violence (victimization and perpetration) in two South African provinces, socio-demographic factors associated with these experiences, and associations with HIV serostatus.
Methods and Findings
In a cross-sectional study conducted in 2008, men aged 18–49 y from randomly selected households in the Eastern Cape and KwaZulu-Natal provinces provided anonymous survey data and dried blood spots for HIV serostatus assessment. Interviews were completed in 1,737 of 2,298 (75.6%) of enumerated and eligible households. From these households, 1,705 men (97.1%) provided data on lifetime history of same-sex experiences, and 1,220 (70.2%) also provided dried blood spots for HIV testing. 5.4% (n = 92) of participants reported a lifetime history of any consensual sexual activity with another man; 9.6% (n = 164) reported any sexual victimization by a man, and 3.0% (n = 51) reported perpetrating sexual violence against another man. 85.0% (n = 79) of men with a history of consensual sex with men reported having a current female partner, and 27.7% (n = 26) reported having a current male partner. Of the latter, 80.6% (n = 21/26) also reported having a female partner. Men reporting a history of consensual male–male sexual behavior are more likely to have been a victim of male-on-male sexual violence (adjusted odds ratio [aOR] = 7.24; 95% CI 4.26–12.3), and to have perpetrated sexual violence against another man (aOR = 3.10; 95% CI 1.22–7.90). Men reporting consensual oral/anal sex with a man were more likely to be HIV+ than men with no such history (aOR = 3.11; 95% CI 1.24–7.80). Men who had raped a man were more likely to be HIV+ than non-perpetrators (aOR = 3.58; 95% CI 1.17–10.9).
Conclusions
In this sample, one in 20 men (5.4%) reported lifetime consensual sexual contact with a man, while about one in ten (9.6%) reported experience of male-on-male sexual violence victimization. Men who reported having had sex with men were more likely to be HIV+, as were men who reported perpetrating sexual violence towards other men. Whilst there was no direct measure of male–female concurrency (having overlapping sexual relationships with men and women), the data suggest that this may have been common. These findings suggest that HIV prevention messages regarding male–male sex in South Africa should be mainstreamed with prevention messages for the general population, and sexual health interventions and HIV prevention interventions for South African men should explicitly address male-on-male sexual violence.
Please see later in the article for the Editors' Summary
Editors' Summary
Background
AIDS first emerged in the early 1980s among gay men living in the US, but it soon became clear that AIDS also infects heterosexual men and women. Now, three decades on, globally, 34 million people (two-thirds of whom live in sub-Saharan Africa and half of whom are women) are infected with HIV, the virus that causes AIDS, and 2.5 million people become infected every year. HIV is most often spread by having unprotected sex with an infected partner, and most sexual transmission of HIV now occurs during heterosexual sex. However, 5%–10% of all new HIV infections still occur in men who have sex with men (MSM; homosexual, bisexual, and transgender men, and heterosexual men who sometimes have consensual sex with men). Moreover, in the concentrated HIV epidemics of high-income countries (epidemics in which the prevalence of HIV infection is more than 5% in at-risk populations such as sex workers but less than 1% in the general population), male-to-male sexual contact remains the most important transmission route, and MSM often have a higher prevalence of HIV infection than heterosexual men.
Why Was This Study Done?
By contrast to high-income countries, HIV epidemics in sub-Saharan Africa are generalized—the prevalence of HIV infection is 1% or more in the general population. Because male-to-male sexual behavior is criminalized in many African countries and because homosexuality is widely stigmatized, little is known about the prevalence of consensual male–male sexual behavior in sub-Saharan Africa. This information and a better understanding of male–female sexual concurrency (having overlapping sexual relationships with men and women) and of how male-to-male transmission contributes to generalized HIV epidemics is needed to inform the design of HIV prevention strategies for use in sub-Saharan Africa. In addition, very little is known about male-on-male sexual violence. Such violence is potentially important to study because we know that male-on-female violence is associated with increased HIV risk for both victims and perpetrators. In this cross-sectional study (an investigation that measures population characteristics at a single time point), the researchers use data from a population-based household survey to investigate the lifetime prevalence of consensual male–male sexual behavior and male-on-male sexual violence (victimization and perpetration) among men in South Africa and the association of these experiences with HIV infection.
What Did the Researchers Do and Find?
About 1,700 adult men from randomly selected households in the Eastern Cape and KwaZulu-Natal provinces of South Africa self-completed a survey that included questions about their lifetime history of same-sex experiences using audio-enhanced personal digital assistants, a data collection method that provided a totally private and anonymous environment for the disclosure of illegal and stigmatized behavior; 1,220 of them also provided dried blood spots for HIV testing. Ninety-two men (5.4% of the participants) reported consensual sexual activity (for example, anal or oral sex) with another man at some time during their life; 9.6% of the men reported that they had been forced to have sex with another man (sexual victimization), and 3% reported that they had perpetrated sexual violence against another man. Most of the men who reported consensual sex with men, including those with current male partners, reported that they had a current female partner. Men with a history of consensual male–male sexual behavior were more likely to have been a victim or perpetrator of male-on-male sexual violence than men without a history of such experiences. Finally, men who reported consensual oral or anal sex with a man were more likely to be HIV+ than men without such a history, and perpetrators of male-on-male sexual violence were more likely to be HIV+ than non-perpetrators.
What Do These Findings Mean?
These findings provide new information about male–male sexual behaviors, male-on-male sexual violence, male–female concurrency, and HIV prevalence among men in two South African provinces. The precision of these findings is likely to be affected by the small numbers of men reporting a history of consensual male–male sexual behavior and of male-on-male sexual violence. Importantly, because the study was cross-sectional, these findings cannot indicate whether the association between consensual male–male sexual behaviors and increased risk of male-on-male sexual violence is causal. Moreover, these findings may not be generalizable to other regions of South Africa or to other African countries. Nevertheless, these findings suggest that information about the risks of male–male sexual behaviors should be included in HIV prevention strategies targeted at the general population in South Africa and that HIV prevention interventions for South African men should explicitly address male-on-male sexual violence. Similar HIV prevention strategies may also be suitable for other African countries, but are likely to succeed only in countries that have, like South Africa, decriminalized consensual homosexual behavior.
Additional Information
Please access these websites via the online version of this summary at http://dx.doi.org/10.1371/journal.pmed.1001472.
This study is further discussed in a PLOS Medicine Perspective by Jerome Singh
Information is available from the US National Institute of Allergy and Infectious Diseases on HIV infection and AIDS
NAM/aidsmap provides basic information about HIV/AIDS, including summaries of recent research findings on HIV care and treatment
Information is available from Avert, an international AIDS charity, on many aspects of HIV/AIDS, including information on HIV and men who have sex with men, on HIV prevention, and on AIDS in Africa (in English and Spanish)
The US Centers for Disease Control and Prevention also has information about HIV/AIDS among men who have sex with men (in English and Spanish)
Patient stories about living with HIV/AIDS are available through Avert; the charity website Healthtalkonline also provides personal stories about living with HIV
doi:10.1371/journal.pmed.1001472
PMCID: PMC3708702  PMID: 23853554
8.  Sexual conflict predicts morphology and behavior in two species of penduline tits 
Background
The evolutionary interests of males and females rarely coincide (sexual conflict), and these conflicting interests influence morphology, behavior and speciation in various organisms. We examined consequences of variation in sexual conflict in two closely-related passerine birds with contrasting breeding systems: the Eurasian penduline tit Remiz pendulinus (EPT) exhibiting a highly polygamous breeding system with sexually antagonistic interests over parental care, and the socially monogamous Cape penduline tit Anthoscopus minutus (CPT). We derived four a priori predictions from sexual conflict theory and tested these using data collected in Central Europe (EPT) and South Africa (CPT). Firstly, we predicted that EPTs exhibit more sexually dimorphic plumage than CPTs due to more intense sexual selection. Secondly, we expected brighter EPT males to provide less care than duller males. Thirdly, since song is a sexually selected trait in many birds, male EPTs were expected to exhibit more complex songs than CPT males. Finally, intense sexual conflict in EPT was expected to lead to low nest attendance as an indication of sexually antagonistic interests, whereas we expected more cooperation between parents in CPT consistent with their socially monogamous breeding system.
Results
Consistent with our predictions EPTs exhibited greater sexual dimorphism in plumage and more complex song than CPTs, and brighter EPT males provided less care than duller ones. EPT parents attended the nest less frequently and less simultaneously than CPT parents.
Conclusions
These results are consistent with sexual conflict theory: species in which sexual conflict is more manifested (EPT) exhibited a stronger sexual dimorphism and more elaborated sexually selected traits than species with less intense sexual conflict (CPT). Our results are also consistent with the notion that EPTs attempt to force their partner to work harder as expected under sexual conflict: each member of the breeding pair attempts to shift the costs of care to the other parent. More brightly colored males benefit more from desertion than dull ones, because they are more likely to remate with a new female. Taken together, the comparison between two closely related species with contrasting breeding systems suggest that sexual conflict over care has influenced the evolution of behavior and morphology in penduline tits.
doi:10.1186/1471-2148-10-107
PMCID: PMC2873415  PMID: 20416066
9.  Hemiclonal analysis of interacting phenotypes in male and female Drosophila melanogaster 
Background
Identifying the sources of variation in mating interactions between males and females is important because this variation influences the strength and/or the direction of sexual selection that populations experience. While the origins and effects of variation in male attractiveness and ornamentation have received much scrutiny, the causes and consequences of intraspecific variation in females have been relatively overlooked. We used cytogenetic cloning techniques developed for Drosophila melanogaster to create “hemiclonal” males and females with whom we directly observed sexual interaction between individuals of different known genetic backgrounds and measured subsequent reproductive outcomes. Using this approach, we were able to quantify the genetic contribution of each mate to the observed phenotypic variation in biologically important traits including mating speed, copulation duration, and subsequent offspring production, as well as measure the magnitude and direction of intersexual genetic correlation between female choosiness and male attractiveness.
Results
We found significant additive genetic variation contributing to mating speed that can be attributed to male genetic identity, female genetic identity, but not their interaction. Furthermore we found that phenotypic variation in copulation duration had a significant male-associated genetic component. Female genetic identity and the interaction between male and female genetic identity accounted for a substantial amount of the observed phenotypic variation in egg size. Although previous research predicts a trade-off between egg size and fecundity, this was not evident in our results. We found a strong negative genetic correlation between female choosiness and male attractiveness, a result that suggests a potentially important role for sexually antagonistic alleles in sexual selection processes in our population.
Conclusion
These results further our understanding of sexual selection because they identify that genetic identity plays a significant role in phenotypic variation in female behaviour and fecundity. This variation may be potentially due to ongoing sexual conflict found between the sexes for interacting phenotypes. Our unexpected observation of a negative correlation between female choosiness and male attractiveness highlights the need for more explicit theoretical models of genetic covariance to investigate the coevolution of female choosiness and male attractiveness.
doi:10.1186/1471-2148-14-95
PMCID: PMC4101844  PMID: 24884361
Sexual selection; Mate choice; Female choosiness; Male attractiveness; Drosophila melanogaster; Hemiclonal analysis; Interacting phenotypes; Mating speed
10.  Multivariate sexual selection in a rapidly evolving speciation phenotype 
Estimating the fitness surface of rapidly evolving secondary sexual traits can elucidate the origins of sexual isolation and thus speciation. Evidence suggests that sexual selection is highly complex in nature, often acting on multivariate sexual characters that sometimes include non-heritable components of variation, thus presenting a challenge for predicting patterns of sexual trait evolution. Laupala crickets have undergone an explosive species radiation marked by divergence in male courtship song and associated female preferences, yet patterns of sexual selection that might explain this diversification remain unknown. We used female phonotaxis trials to estimate the fitness surface for acoustic characters within one population of Laupala cerasina, a species with marked geographical variation in male song and female preferences. Results suggested significant directional sexual selection on three major song traits, while canonical rotation of the matrix of nonlinear selection coefficients (γ) revealed the presence of significant convex (stabilizing) sexual selection along combinations of characters. Analysis of song variation within and among males indicated significantly higher repeatability along the canonical axis of greatest stabilizing selection than along the axis of greatest linear selection. These results are largely consistent with patterns of song divergence that characterize speciation and suggest that different song characters have the potential to indicate distinct information to females during courtship.
doi:10.1098/rspb.2013.0482
PMCID: PMC3652440  PMID: 23760640
female preference; acoustic signalling; stabilizing selection; fitness surface; repeatability; Laupala
11.  RUNAWAY SEXUAL SELECTION WITHOUT GENETIC CORRELATIONS: SOCIAL ENVIRONMENTS AND FLEXIBLE MATE CHOICE INITIATE AND ENHANCE THE FISHER PROCESS 
Female mating preferences are often flexible, reflecting the social environment in which they are expressed. Associated indirect genetic effects (IGEs) can affect the rate and direction of evolutionary change, but sexual selection models do not capture these dynamics. We incorporate IGEs into quantitative genetic models to explore how variation in social environments and mate choice flexibility influence Fisherian sexual selection. The importance of IGEs is that runaway sexual selection can occur in the absence of a genetic correlation between male traits and female preferences. Social influences can facilitate the initiation of the runaway process and increase the rate of trait elaboration. Incorporating costs to choice do not alter the main findings. Our model provides testable predictions: (1) genetic covariances between male traits and female preferences may not exist, (2) social flexibility in female choice will be common in populations experiencing strong sexual selection, (3) variation in social environments should be associated with rapid sexual trait divergence, and (4) secondary sexual traits will be more elaborate than previously predicted. Allowing feedback from the social environment resolves discrepancies between theoretical predictions and empirical data, such as why indirect selection on female preferences, theoretically weak, might be sufficient for preferences to become elaborated.
doi:10.1111/j.1558-5646.2012.01647.x
PMCID: PMC3627302  PMID: 22946795
Fisherian runaway; indirect genetic effects; interacting phenotypes; mate choice plasticity; mate preference learning; social evolution
12.  Causes of male sexual trait divergence in introduced populations of guppies 
Journal of Evolutionary Biology  2014;27(2):437-448.
Males from different populations of the same species often differ in their sexually selected traits. Variation in sexually selected traits can be attributed to sexual selection if phenotypic divergence matches the direction of sexual selection gradients among populations. However, phenotypic divergence of sexually selected traits may also be influenced by other factors, such as natural selection and genetic constraints. Here, we document differences in male sexual traits among six introduced Australian populations of guppies and untangle the forces driving divergence in these sexually selected traits. Using an experimental approach, we found that male size, area of orange coloration, number of sperm per ejaculate and linear sexual selection gradients for male traits differed among populations. Within populations, a large mismatch between the direction of selection and male traits suggests that constraints may be important in preventing male traits from evolving in the direction of selection. Among populations, however, variation in sexual selection explained more than half of the differences in trait variation, suggesting that, despite within-population constraints, sexual selection has contributed to population divergence of male traits. Differences in sexual traits were also associated with predation risk and neutral genetic distance. Our study highlights the importance of sexual selection in trait divergence in introduced populations, despite the presence of constraining factors such as predation risk and evolutionary history.
doi:10.1111/jeb.12313
PMCID: PMC4237193  PMID: 24456226
alignment; coloration; genetic drift; introduced populations; natural selection; Poecilia reticulata; population divergence; predation; selection gradient; sexual selection
13.  Sexual responsiveness is condition-dependent in female guppies, but preference functions are not 
BMC Ecology  2004;4:5.
Background
Variation in mate choice behaviour among females within a population may influence the strength and form of sexual selection, yet the basis for any such variation is still poorly understood. Condition-dependence may be an important source of variation in female sexual responsiveness and in the preference functions for male display traits that she expresses when choosing. We manipulated food intake of female guppies (Poecilia reticulata), and examined the effect on several measures of condition and various components of mate choice behaviour.
Results
Diet significantly influenced four measures of female condition: standard length, weight, reproductive status and somatic fat reserves. Diet also significantly affected female sexual responsiveness, but not preference functions: females in good and poor condition prefer the same males.
Conclusions
Variation in female condition within populations is therefore unlikely to influence the direction of sexual selection imposed by female choice. It may, however, influence the strength of sexual selection due to its effects on female responsiveness. The relative importance of female choice as a sexually selective force may also covary with female condition, however, because low responsiveness may result in sneak copulations being relatively more important as a determinant of the paternity of offspring. Differences among populations in mean condition may also influence geographic differences in the strength of sexual selection.
doi:10.1186/1472-6785-4-5
PMCID: PMC411045  PMID: 15117410
14.  Ejaculate-female coevolution in Drosophila mojavensis. 
Interspecific studies indicate that sperm morphology and other ejaculatory traits diverge more rapidly than other types of character in Drosophila and other taxa. This pattern has largely been attributed to postcopulatory sexual selection involving interaction between the sexes. Such divergence has been suggested to lead rapidly to reproductive isolation among populations and thus to be an 'engine of speciation.' Here, we test two critical predictions of this hypothesis: (i) there is significant variation in reproductive traits among incipient species; and (ii) divergence in interacting sex-specific traits exhibits a coevolutionary pattern among populations within a species, by examining geographical variation in Drosophila mojavensis, a species in the early stages of speciation. Significant among-population variation was identified in sperm length and female sperm-storage organ length, and a strong pattern of correlated evolution between these interacting traits was observed. In addition, crosses among populations revealed coevolution of male and female contributions to egg size. Support for these two important predictions confirms that coevolving internal characters that mediate successful reproduction may play an important part in speciation. The next step is to determine exactly what that role is.
doi:10.1098/rspb.2003.2382
PMCID: PMC1691392  PMID: 12965017
15.  Genetics of decayed sexual traits in a parasitoid wasp with endosymbiont-induced asexuality 
Heredity  2014;113(5):424-431.
Trait decay may occur when selective pressures shift, owing to changes in environment or life style, rendering formerly adaptive traits non-functional or even maladaptive. It remains largely unknown if such decay would stem from multiple mutations with small effects or rather involve few loci with major phenotypic effects. Here, we investigate the decay of female sexual traits, and the genetic causes thereof, in a transition from haplodiploid sexual reproduction to endosymbiont-induced asexual reproduction in the parasitoid wasp Asobara japonica. We take advantage of the fact that asexual females cured of their endosymbionts produce sons instead of daughters, and that these sons can be crossed with sexual females. By combining behavioral experiments with crosses designed to introgress alleles from the asexual into the sexual genome, we found that sexual attractiveness, mating, egg fertilization and plastic adjustment of offspring sex ratio (in response to variation in local mate competition) are decayed in asexual A. japonica females. Furthermore, introgression experiments revealed that the propensity for cured asexual females to produce only sons (because of decayed sexual attractiveness, mating behavior and/or egg fertilization) is likely caused by recessive genetic effects at a single locus. Recessive effects were also found to cause decay of plastic sex-ratio adjustment under variable levels of local mate competition. Our results suggest that few recessive mutations drive decay of female sexual traits, at least in asexual species deriving from haplodiploid sexual ancestors.
doi:10.1038/hdy.2014.43
PMCID: PMC4220718  PMID: 24781809
16.  Family feuds: social competition and sexual conflict in complex societies 
Darwin was initially puzzled by the processes that led to ornamentation in males—what he termed sexual selection—and those that led to extreme cooperation and altruism in complex animal societies—what was later termed kin selection. Here, I explore the relationships between sexual and kin selection theory by examining how social competition for reproductive opportunities—particularly in females—and sexual conflict over mating partners are inherent and critical parts of complex altruistic societies. I argue that (i) patterns of reproductive sharing within complex societies can drive levels of social competition and reproductive conflict not only in males but also in females living in social groups, and ultimately the evolution of female traits such as ornaments and armaments; (ii) mating conflict over female choice of sexual partners can influence kin structure within groups and drive the evolution of complex societies; and (iii) patterns of reproductive sharing and conflict among females may also drive the evolution of complex societies by influencing kin structure within groups. Ultimately, complex societies exhibiting altruistic behaviour appear to have only arisen in taxa where social competition over reproductive opportunities and sexual conflict over mating partners were low. Once such societies evolved, there were important selective feedbacks on traits used to regulate and mediate intra-sexual competition over reproductive opportunities, particularly in females.
doi:10.1098/rstb.2011.0283
PMCID: PMC3391424  PMID: 22777018
kin selection; sexual selection; social selection; sexual conflict; reproductive conflict; mating conflict
17.  A potential resolution to the lek paradox through indirect genetic effects 
Females often prefer males with elaborate traits, even when they receive no direct benefits from their choice. In such situations, mate discrimination presumably has genetic advantages; selective females will produce offspring of higher genetic quality. Over time, persistent female preferences for elaborate secondary-sexual traits in males should erode genetic variance in these traits, eventually eliminating any benefit to the preferences. Yet, strong female preferences persist in many taxa. This puzzle is called the lek paradox and raises two primary questions: do females obtain genetic benefits for offspring by selecting males with elaborate secondary-sexual characteristics and, if so, how is the genetic variation in these male traits maintained? We suggest that indirect genetic effects may help to resolve the lek paradox. Maternal phenotypes, such as habitat selection behaviours and offspring provisioning, often influence the condition and the expression of secondary-sexual traits in sons. These maternal influences are commonly genetic based (i.e. they are indirect genetic effects). Females choosing mates with elaborate traits may receive ‘good genes’ for daughters in the form of effective maternal characteristics. Recognizing the significance of indirect genetic effects may be important to our understanding of the process and consequences of sexual selection.
doi:10.1098/rspb.2006.0413
PMCID: PMC2176171  PMID: 17341455
lek paradox; indirect genetic effects; sexual selection; condition dependence; good genes; maternal effects
18.  Quantitative genetic insights into the coevolutionary dynamics of male and female genitalia 
The spectacular variability that typically characterizes male genital traits has largely been attributed to the role of sexual selection. Among the evolutionary mechanisms proposed to account for this diversity, two processes in particular have generated considerable interest. On the one hand, females may exploit postcopulatory mechanisms of selection to favour males with preferred genital traits (cryptic female choice; CFC), while on the other hand females may evolve structures or behaviours that mitigate the direct costs imposed by male genitalia (sexual conflict; SC). A critical but rarely explored assumption underlying both processes is that male and female reproductive traits coevolve, either via the classic Fisherian model of preference-trait coevolution (CFC) or through sexually antagonistic selection (SC). Here, we provide evidence for this prediction in the guppy (Poecilia reticulata), a polyandrous livebearing fish in which males transfer sperm internally to females via consensual and forced matings. Our results from a paternal half-sibling breeding design reveal substantial levels of additive genetic variation underlying male genital size and morphology—two traits known to predict mating success during non-consensual matings. Our subsequent finding that physically interacting female genital traits exhibit corresponding levels of genetic (co)variation reveals the potential intersexual coevolutionary dynamics of male and female genitalia, thereby fulfilling a fundamental assumption underlying CFC and SC theory.
doi:10.1098/rspb.2013.0749
PMCID: PMC3774229  PMID: 23720546
sperm competition; genetic correlation; heritability; genital evolution
19.  A Cost of Sexual Attractiveness to High-Fitness Females 
PLoS Biology  2009;7(12):e1000254.
Females are frequently harassed and harmed by males attempting to obtain matings. When these males are also “choosy” with their courtship, there may be negative consequences to the species' ability to adaptively evolve.
Adaptive mate choice by females is an important component of sexual selection in many species. The evolutionary consequences of male mate preferences, however, have received relatively little study, especially in the context of sexual conflict, where males often harm their mates. Here, we describe a new and counterintuitive cost of sexual selection in species with both male mate preference and sexual conflict via antagonistic male persistence: male mate choice for high-fecundity females leads to a diminished rate of adaptive evolution by reducing the advantage to females of expressing beneficial genetic variation. We then use a Drosophila melanogaster model system to experimentally test the key prediction of this theoretical cost: that antagonistic male persistence is directed toward, and harms, intrinsically higher-fitness females more than it does intrinsically lower-fitness females. This asymmetry in male persistence causes the tails of the population's fitness distribution to regress towards the mean, thereby reducing the efficacy of natural selection. We conclude that adaptive male mate choice can lead to an important, yet unappreciated, cost of sex and sexual selection.
Author Summary
In many species, females are frequently subject to harassing courtship from males attempting to mate with them. These persistent male behaviors can result in females incurring substantial direct fitness costs. We set out to examine how these costs may influence adaptive potential in a species that also exhibits male mate choice, i.e., a preference by males for females exhibiting certain traits. We found that harmful courtship behaviors were directed predominantly towards females of greater reproductive potential (and away from females of lesser potential), resulting in a reduction in the variation of lifetime reproductive successes among females in the population. This change in distribution of realized fitnesses represents a previously unappreciated consequence of sexual conflict–adaptive male mate preference can slow the rate of accumulation of beneficial mutations and speed the rate of accumulation of harmful mutations, thereby creating a “sexual conflict adaptive load” within a species.
doi:10.1371/journal.pbio.1000254
PMCID: PMC2780925  PMID: 19997646
20.  Sexual selection, germline mutation rate and sperm competition 
Background
An important component of sexual selection arises because females obtain viability benefits for their offspring from their mate choice. Females choosing extra-pair fertilization generally favor males with exaggerated secondary sexual characters, and extra-pair paternity increases the variance in male reproductive success. Furthermore, females are assumed to benefit from 'good genes' from extra-pair sires. How additive genetic variance in such viability genes is maintained despite strong directional selection remains an evolutionary enigma. We propose that sexual selection is associated with elevated mutation rates, changing the balance between mutation and selection, thereby increasing variance in fitness and hence the benefits to be obtained from good genes sexual selection. Two hypotheses may account for such elevated mutation: (1) Increased sperm production associated with sperm competition may increase mutation rate. (2) Mutator alleles increase mutation rates that are revealed by the expression of condition-dependent secondary sexual characters used by choosy females during their mate choice. M Petrie has independently developed the idea that mutator alleles may account for the maintenance of genetic variation in viability despite strong directional selection.
Results
A comparative study of birds revealed a positive correlation between mutation rate at minisatellite loci and extra-pair paternity, but not between mutation rate and relative testes mass which is a measure of relative sperm production. Minisatellite mutation rates were not related to longevity, suggesting a meiotic rather than a mitotic origin of mutations.
Conclusion
We found evidence of increased mutation rate in species with more intense sexual selection. Increased mutation was not associated with increased sperm production, and we suggest that species with intense sexual selection may maintain elevated mutation rates because sexual selection continuously benefits viability alleles expressed in condition-dependent characters. Sexual selection may increase mutational input, which in turn feeds back on sexual selection because of increased variance in viability traits.
doi:10.1186/1471-2148-3-6
PMCID: PMC156621  PMID: 12702218
birds; extra-pair paternity; minisatellites; sex-biased mutation; sperm
21.  Direct selection on male attractiveness and female preference fails to produce a response 
Background
Theoretical studies suggest that direct and indirect selection have the potential to cause substantial evolutionary change in female mate choice. Similarly, sexual selection is considered a strong force in the evolution of male attractiveness and the exaggeration of secondary sexual traits. Few studies have, however, directly tested how female mate choice and male attractiveness respond to selection. Here we report the results of a selection experiment in which we selected directly on female mating preference for attractive males and, independently, on male attractiveness in the guppy, Poecilia reticulata. We measured the direct and correlated responses of female mate choice and male attractiveness to selection and the correlated responses of male ornamental traits, female fecundity and adult male and female survival.
Results
Surprisingly, neither female mate choice nor male attractiveness responded significantly to direct or to indirect selection. Fecundity did differ significantly among lines in a way that suggests a possible sexually-antagonistic cost to male attractiveness.
Conclusions
The opportunity for evolutionary change in female mate choice and male attractiveness may be much smaller than predicted by current theory, and may thus have important consequences for how we understand the evolution of female mate choice and male attractiveness. We discuss a number of factors that may have constrained the response of female choice and male attractiveness to selection, including low heritabilities, low levels of genetic (co)variation in the multivariate direction of selection, sexually-antagonistic constraint on sexual selection and the "environmental covariance hypothesis".
doi:10.1186/1471-2148-4-1
PMCID: PMC319700  PMID: 14720309
preference function; sexual selection; quantitative genetics; realized heritability; genetic correlation; sexually antagonistic genes; lek paradox
22.  Sex-specific effects of developmental environment on reproductive trait expression in Drosophila melanogaster 
Ecology and Evolution  2012;2(7):1362-1370.
Variation in the expression of reproductive traits provides the raw material upon which sexual selection can act. It is therefore important to understand how key factors such as environmental variation influence the expression of reproductive traits, as these will have a fundamental effect on the evolution of mating systems. It is also important to consider the effects of environmental variation upon reproductive traits in both sexes and to make comparisons with the environment to which the organism is adapted. In this study, we addressed these issues in a systematic study of the effect of a key environmental factor, variation in larval density, on reproductive trait expression in male and female Drosophila melanogaster. To do this, we compared reproductive trait expression when flies were reared under controlled conditions at eight different larval densities that covered a 20-fold range. Then, to place these results in a relevant context, we compared the results to those from flies sourced directly from stock cages. Many reproductive traits were surprisingly insensitive to variation in larval density. A notable exception was nonlinear variation in female fecundity. In contrast, we found much bigger differences in comparisons with flies from stock cages—including differences in body size, latency to mate, copulation duration, fecundity, and male share of paternity in a competitive environment. For a number of traits, even densities of 1000 larvae per vial (125 larvae per mL of food) did not phenocopy stock cage individuals. This study reveals novel patterns of sex-specific sensitivity to environmental variation that will influence the strength of sexual selection. It also illustrates the importance of comparisons with the environment to which individuals are adapted.
doi:10.1002/ece3.243
PMCID: PMC3434946  PMID: 22957145
Drosophila melanogaster; environmental variation; genotype-by-environment interaction; larval density; larval development; sexual selection
23.  Adult locomotory activity mediates intralocus sexual conflict in a laboratory-adapted population of Drosophila melanogaster 
The strongest form of intralocus sexual conflict occurs when two conditions are met: (i) there is a positive intersexual genetic correlation for a trait and (ii) the selection gradients on the trait in the two sexes are in opposite directions. Intralocus sexual conflict can constrain the adaptive evolution of both sexes and thereby contribute to a species' ‘gender load’. Previous studies of adult lifetime fitness of the same sets of genes expressed in both males and females have established that there is substantial intralocus conflict in the LHM laboratory-adapted population of Drosophila melanogaster. Here, we investigated whether a highly dimorphic trait—adult locomotory activity—contributed substantially to the established intralocus sexual conflict. To measure the selection gradient on activity level, both this trait and adult lifetime fitness were measured under the same environmental conditions to which the flies were adapted. We found significant phenotypic variation in both sexes for adult locomotory activity, and that the selection gradients on this variation were large and in opposite directions in the two sexes. Using hemiclonal analysis to screen 99% of the entire genome, we found abundant genetic variation for adult locomotory activity and showed that this variation occurs on both the X and autosomes. We also established that there is a strong positive intersexual genetic correlation for locomotory activity. These assays revealed that, despite the strong, extant sexual dimorphism for the trait, locomotory activity continues to contribute strongly to intralocus sexual conflict in this population.
doi:10.1098/rspb.2007.1140
PMCID: PMC2293944  PMID: 17925279
intralocus sexual conflict; sexually antagonistic alleles; gender load; locomotory activity; sex chromosomes; fitness
24.  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.
doi:10.1098/rspb.2010.2272
PMCID: PMC3107629  PMID: 21159677
maternal investment; fecundity; egg size; differential allocation hypothesis; sexual conflict; Drosophila melanogaster
25.  Remating and Sperm Competition in Replicate Populations of Drosophila melanogaster Adapted to Alternative Environments 
PLoS ONE  2014;9(2):e90207.
The prevalence of sexual conflict in nature, as well as the supposedly arbitrary direction of the resulting coevolutionary trajectories, suggests that it may be an important driver of phenotypic divergence even in a constant environment. However, natural selection has long been central to the operation of sexual conflict within populations and may therefore constrain or otherwise direct divergence among populations. Ecological context may therefore matter with respect to the diversification of traits involved in sexual conflict, and if natural selection is sufficiently strong, such traits may evolve in correlation with environment, generating a pattern of ecologically-dependent parallel evolution. In this study we assess among-population divergence both within and between environments for several traits involved in sexual conflict. Using eight replicate populations of Drosophila melanogaster from a long-term evolution experiment, we measured remating rates and subsequent offspring production of females when housed with two separate males in sequence. We found no evidence of any variation in male reproductive traits (offense or defense). However, the propensity of females to remate diverged significantly among the eight populations with no evidence of any environmental effect, consistent with sexual conflict promoting diversification even in the absence of ecological differences. On the other hand, females adapted to one environment (ethanol) tended to produce a higher proportion of offspring sired by their first mate as compared to those adapted to the other (cadmium) environment, suggesting ecologically-based divergence of this conflict phenotype. Because we find evidence for both stochastic population divergence operating outside of an ecological context and environment-dependent divergence of traits under sexual conflict, the interaction of these two processes is an important topic for future work.
doi:10.1371/journal.pone.0090207
PMCID: PMC3934985  PMID: 24587283

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