Directional Sexual Selection Research Articles

Transcriptomic sexual conflict at two evolutionary timescales revealed by experimental evolution in Caenorhabditis elegans.

Sex-specific regulation of gene expression is the most plausible way for generating sexually differentiated phenotypes from an essentially shared genome. However, since genetic material is shared, sex-specific selection in one sex can have an indirect response in the other sex. From a gene expression perspective, this tethered response can move one sex away from their wildtype expression state and impact potentially many gene regulatory networks. Here, using experimental evolution in the model nematode Caenorhabditis elegans, we explore the coupling of direct sexual selection on males with the transcriptomic response in males and females over microevolutionary timescales to uncover the extent to which post-insemination reproductive traits share a genetic basis between the sexes. We find that differential gene expression evolved in a sex-specific manner in males, while in females indirect selection causes an evolved response. Almost all differentially expressed genes were downregulated in both evolved males and females. Moreover, 97% of significantly differentially expressed genes in males and 69% of significantly differentially expressed genes in females have wildtype female-biased expression profile. Changes in gene expression profiles were likely driven through trans -acting pathways that are shared between the sexes. We found no evidence that the core dosage compensation machinery was impacted by experimental evolution. Together these data suggest a de-feminization of the male transcriptome and masculinization of the female transcriptome driven by direct selection on male sperm competitive ability. Our results indicate that on short evolutionary timescales sexual selection can generate putative sexual conflict in expression space.

Strength of Sexual Selection and Sex Roles Vary between Social Groups in a Coral Reef Cardinalfish.

AbstractThe strength and direction of sexual selection can vary among populations. However, spatial variability is rarely explored at the level of the social group. Here we investigate sexual selection and sex roles in the paternally mouthbrooding, socially monogamous, and site-attached pajama cardinalfish, Sphaeramia nematoptera. Females were larger and more aggressive and had a longer dorsal fin filament, indicating reversed sex roles. At the scale of social groups, we show that the Bateman gradient and reproductive variance depend on the sex ratio and size of groups. In small and medium-sized groups with balanced or male-biased sex ratios, Bateman gradients were steeper for females, whereas gradients were equally steep for both sexes in large groups or when the sex ratio was female biased. For both sexes, reproductive variance increased with group size and with a higher male-to-female sex ratio. In S. nematoptera, mating opportunities outside the socially monogamous pair appear to impact sexual selection. We conclude that strength and direction of sexual selection can be masked by social dynamics in group-living species when considering only population and large-scale demographic processes.

Population density effects on gamete traits and fertilisation dynamics under varying sperm environments in mussels.

Gamete traits can vary widely among species, populations and individuals, influencing fertilisation dynamics and overall reproductive fitness. Sexual selection can play an important role in determining the evolution of gamete traits with local environmental conditions determining the strength and direction of sexual selection. Here, we test for signatures of post-mating selection on gamete traits in relation to population density, and possible interactive effects of population density and sperm concentration on sperm motility and fertilisation rates among natural populations of mussels. Our study shows that males from high-density populations produce smaller sperm compared with males from low-density populations, but we detected no effect of population density on egg size. Our results also reveal that females from low-density populations tended to exhibit lower fertilisation rates across a range of sperm concentrations, although this became less important as sperm concentration increased. Variances in fertilisation success were higher for females than males and the effect of gamete compatibility between males and females increases as sperm concentrations increase. These results suggest that local population density can influence gamete traits and fertilisation dynamics but also highlight the importance of phenotypic plasticity in governing sperm-egg interactions in a highly dynamic selective environment.

Female and male plumage brightness is positively correlated among populations of the dichromatic Variable Seedeater

Abstract Because studies of plumage coloration often focus on highly elaborate and conspicuous males, little is known about the factors driving theevolution of drab plumage in females of dichromatic species. We explored variation in the color properties of drab female plumage across subspecies of the Variable Seedeater (Sporophila corvina) and found a correlation between plumage brightness of male and female plumage patches. This correlation is consistent with the hypothesis that differences in plumage brightness among females result, at least partially, from a genetic correlation or shared developmental pathway with the more conspicuous male plumage traits that are shaped by sexual selection. Furthermore, we modeled the perception of female plumage using the avian visual system and found that most of the variation in color among females is undetectable by birds; therefore, it is unlikely for such variation to have evolved via direct sexual selection as a signal for recognition or assortative mating. Together, these results suggest that variation in S. corvina female color result from non-adaptive processes. However, we found a reduced variation on color of dorsal patches compared with that of ventral patches among females, which could be explained by natural selection on crypsis, reducing the variation on dorsal patches. Finally, we found little differences in plumage color between adult females and juveniles, which suggest selection for juveniles to resemble adult females possibly to reduce aggression from adult males. Additional within-population studies and behavioral experiments are needed to discern the evolutionary factors driving variation on S. corvina female color and its function.

Strongly sexually dimorphic forelegs are not more condition-dependent than less dimorphic traits in Drosophila prolongata

Directional sexual selection drives the evolution of traits that are most closely linked to reproductive success, giving rise to trait exaggeration and sexual dimorphism. Exaggerated structures are often costly and, therefore, thought to be expressed in a condition-dependent manner. Sexual selection theory thus predicts a direct link between directional sexual selection, sexual dimorphism, and sex-specific condition dependence. However, only a handful of studies investigate the relationship between sexual dimorphism and condition dependence. Using 21 genetic lines of Drosophila prolongata, we here compared the degree of sexual dimorphism and sex-specific condition dependence, measured as allometric slopes, in sexually selected and non-sexual traits. Our data revealed male-biased sexual dimorphism in all traits examined, most prominently in the sexually selected forelegs. However, there was no relationship between the degree of sex-specific condition dependence and sexual dimorphism across traits and genetic lines. Our results contradict theoretical predictions and highlight the importance of understanding the role of exaggerated traits in the context of both sexual and natural selection.

Cumulative cultural evolution and mechanisms for cultural selection in wild bird songs

Cumulative cultural evolution, the accumulation of sequential changes within a single socially learned behaviour that results in improved function, is prominent in humans and has been documented in experimental studies of captive animals and managed wild populations. Here, we provide evidence that cumulative cultural evolution has occurred in the learned songs of Savannah sparrows. In a first step, “click trains” replaced “high note clusters” over a period of three decades. We use mathematical modelling to show that this replacement is consistent with the action of selection, rather than drift or frequency-dependent bias. Generations later, young birds elaborated the “click train” song form by adding more clicks. We show that the new songs with more clicks elicit stronger behavioural responses from both males and females. Therefore, we suggest that a combination of social learning, innovation, and sexual selection favoring a specific discrete trait was followed by directional sexual selection that resulted in naturally occurring cumulative cultural evolution in the songs of this wild animal population.

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

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

Axes of multivariate sexual signal divergence among incipient species: Concordance with selection, genetic variation and phenotypic plasticity.

Sexual signalling traits are often observed to diverge rapidly among populations, thereby playing a potentially key early role in the evolution of reproductive isolation. While often assumed to reflect divergent sexual selection among populations, patterns of sexual trait diversification might sometimes be biased along axes of standing additive genetic variation and covariation among trait components. Additionally, theory predicts that environmentally induced phenotypic variation might facilitate rapid trait evolution, suggesting that patterns of divergence between populations should mirror phenotypic plasticity within populations. Here, we evaluate the concordance between observed axes of multivariate sexual trait divergence and predicted divergence based on (1) interpopulation variation in sexual selection, (2) additive genetic variances and (3) temperature-related phenotypic plasticity in male courtship song among geographically isolated populations of the Hawaiian swordtail cricket, Laupala cerasina, which exhibit sexual isolation due acoustic signalling traits. The major axis of multivariate divergence, dmax , accounted for 76% of variation among population male song trait means and was moderately correlated with interpopulation differences in directional sexual selection based on female preferences. However, the majority of additive genetic variance was largely oriented away from the direction of divergence, suggesting that standing genetic variation may not play a dominant role in the patterning of signal divergence. In contrast, the axis of phenotypic plasticity strongly mirrored patterns of interpopulation phenotypic divergence, which is consistent with a role for temperature-related plasticity in facilitating instead of inhibiting male song evolution and sexual isolation in these incipient species. We propose potential mechanisms by which sexual selection might interact with phenotypic plasticity to facilitate the rapid acoustic diversification observed in this species and clade.

Smart mating: the cognitive ability of females influences their preference for male cognitive ability.

Cognitive abilities may be crucial for individuals to respond appropriately to their social and natural environment, thereby increasing fitness. However, the role of cognitive traits in sexual selection has received relatively little attention. Here, we studied 1) whether male secondary sexual traits (colour, courtship, and nest) reflect their cognitive ability, 2) whether females choose mates based on males' and their own cognitive abilities, and 3) how the interplay between secondary sexual traits and cognitive ability determines male attractiveness in the three-spined stickleback (Gasterosteus aculetaus). For this, we first evaluated the cognitive ability of sexually mature males and females in a detour-reaching task. Then, female preference was repeatedly assessed in a dichotomous-choice test, where the female was exposed to two males with contrasting performances (relatively good and bad) in the detour-reaching task. Female preference for better performing males was affected by the female's own cognitive ability. Females with relatively medium-low cognitive ability preferred males with high ability, whereas females with high ability showed no preference. We also found that males with higher cognitive abilities built more elaborated nests, but showed weaker red nuptial colouration. To our knowledge, this is among the first results that illustrate how cognitive traits of both sexes influence female mate preference, which has implications for the strength and direction of sexual selection.

Impact of male trait exaggeration on sex-biased gene expression and genome architecture in a water strider

BackgroundExaggerated secondary sexual traits are widespread in nature and often evolve under strong directional sexual selection. Although heavily studied from both theoretical and empirical viewpoints, we have little understanding of how sexual selection influences sex-biased gene regulation during the development of exaggerated secondary sexual phenotypes, and how these changes are reflected in genomic architecture. This is primarily due to the limited availability of representative genomes and associated tissue and sex transcriptomes to study the development of these traits. Here we present the genome and developmental transcriptomes, focused on the legs, of the water strider Microvelia longipes, a species where males exhibit strikingly long third legs compared to females, which they use as weapons.ResultsWe generated a high-quality genome assembly with 90% of the sequence captured in 13 scaffolds. The most exaggerated legs in males were particularly enriched in both sex-biased and leg-biased genes, indicating a specific signature of gene expression in association with trait exaggeration. We also found that male-biased genes showed patterns of fast evolution compared to non-biased and female-biased genes, indicative of directional or relaxed purifying selection. By contrast to male-biased genes, female-biased genes that are expressed in the third legs, but not the other legs, are over-represented in the X chromosome compared to the autosomes. An enrichment analysis for sex-biased genes along the chromosomes revealed also that they arrange in large genomic regions or in small clusters of two to four consecutive genes. The number and expression of these enriched regions were often associated with the exaggerated legs of males, suggesting a pattern of common regulation through genomic proximity in association with trait exaggeration.ConclusionOur findings indicate how directional sexual selection may drive sex-biased gene expression and genome architecture along the path to trait exaggeration and sexual dimorphism.

The Frog Fauna of Southwestern Australia: Diverse, Bizarre, Old, and Polyandrous

My research on anurans has been diverse: biogeography, speciation, acoustics, polyandry, sperm competition, and conservation. My interests in biology started in natural history but, in the late 1960s as an undergraduate student, I was receptive to emerging new ideas in biogeography and evolutionary biology: continental drift and neutral theory. My focus in this “Perspective” is an explanation of how diversity has evolved in the frog fauna of southwestern Australia, where I have worked since 1978. I discuss the roles of range fragmentation, genetic drift, directional sexual selection, polyploidy, and simultaneous polyandry as processes driving the evolution of diversity in the sometimes-bizarre frog fauna of southwestern Australia. I identify features that can characterize polyandrous anurans: e.g., large testes, sperm morphology, and, possibly, complex calls with an example of the latter in Geocrinia leai. I discuss how current anuran life histories vary across rainfall and temperature gradients and how derivation of more-arid adapted forms is a well-defined historic biogeographic pattern in southwestern Australia. My observations over time leave me cautiously optimistic about the prospects for frogs affected by global warming.

Sexual selection after gamete release in broadcast spawning invertebrates.

Broadcast spawning invertebrates offer highly tractable models for evaluating sperm competition, gamete-level mate choice and sexual conflict. By displaying the ancestral mating strategy of external fertilization, where sexual selection is constrained to act after gamete release, broadcast spawners also offer potential evolutionary insights into the cascade of events that led to sexual reproduction in more 'derived' groups (including humans). Moreover, the dynamic reproductive conditions faced by these animals mean that the strength and direction of sexual selection on both males and females can vary considerably. These attributes make broadcast spawning invertebrate systems uniquely suited to testing, extending, and sometimes challenging classic and contemporary ideas in sperm competition, many of which were first captured in Parker's seminal papers on the topic. Here, we provide a synthesis outlining progress in these fields, and highlight the burgeoning potential for broadcast spawners to provide both evolutionary and mechanistic understanding into gamete-level sexual selection more broadly across the animal kingdom. This article is part of the theme issue 'Fifty years of sperm competition'.

Sexually dichromatic coloration of female Iberian green lizards correlates with health state and reproductive investment

Females often have chromatic patterns that differ from those of males. The evolution and function of female coloration is less known than those of males. Female ornaments can result from non-adaptive intersexual genetic correlation, but they may also signal female quality, health state, or potential fecundity. We examined whether the spectral characteristics of the sexually dichromatic coloration of female Iberian green lizards (Lacerta schreiberi) correlate with their condition, parasite load (ticks, hemoparasites and Borrelia infection) and the inflammatory response, and predict reproductive investment and offspring quality. Females with more intense UV-blue throat structural coloration and with more intense carotenoid-dependent yellow chests had less hemoparasites, and females with more saturated green dorsal coloration had lower tick loads. Also, females with greener backs seemed less prone to Borrelia burgdorferi s. l. infection. Surprisingly, in females not infected with Borrelia, there was a negative relationship between tick load and carotenoid content in the chest, which was not obvious in infected females. Characteristics of the females’ coloration may also predict several variables of reproductive investment, such as egg laying date, incubation time, hatchling number, hatching success, and body size and condition of their hatchlings. Because this is a polygynandric species and mating investment is costly for males, we suggest that males might use female coloration to select potential mates. However, we can expect that the physiological basis of coloration is similar in both sexes and, therefore, genetic correlation and sexual selection may act synergistically. Despite widespread misconception that males are brightly colored and females are dull, females of some species also signal their quality with colorful ornaments. However, the function of female coloration is less often studied, although it may be important to fully understand sexual selection. Coloration of female Iberian green lizards is not so bright as that of males, but spectral characteristics of female colors can reflect body condition, parasite load, and immune response and, moreover, predict the number and quality of her future offspring. These correlations might help males to choose among female partners when selecting a good mate is a time and energy demanding task, increasing males’ fitness. This would support direct sexual selection of female ornaments.

How female × male and male × male interactions influence competitive fertilization in Drosophila melanogaster.

How males and females contribute to joint reproductive success has been a long‐standing question in sexual selection. Under postcopulatory sexual selection, paternity success is predicted to derive from complex interactions among females engaging in cryptic female choice and males engaging in sperm competition. Such interactions have been identified as potential sources of genetic variation in sexually selected traits but are also expected to inhibit trait diversification. To date, studies of interactions between females and competing males have focused almost exclusively on genotypes and not phenotypic variation in sexually selected traits. Here, we characterize within‐ and between‐sex interactions in Drosophila melanogaster using isogenic lines with heritable variation in both male and female traits known to influence competitive fertilization. We confirmed, and expanded on, previously reported genotypic interactions within and between the sexes, and showed that several reproductive events, including sperm transfer, female sperm ejection, and sperm storage, were explained by two‐ and three‐way interactions among sex‐specific phenotypes. We also documented complex interactions between the lengths of competing males’ sperm and the female seminal receptacle, which are known to have experienced rapid female‐male co‐diversification. Our results highlight the nonindependence of sperm competition and cryptic female choice and demonstrate that complex interactions between the sexes do not limit the ability of multivariate systems to respond to directional sexual selection.

Habitat deterioration relaxes resource competition and sexual selection in the threespine stickleback

The operation of sexual selection depends on ecological conditions. Thus, changes in environmental conditions because of human activities can alter the strength and direction of sexual selection, with implications for evolutionary trajectories and the viability of populations. We show that aquatic algal blooms can relax the operation of sexual selection by influencing which males are available to attract females. This is by influencing the ability of males to maintain a resource needed in mate attraction. When we exposed two competing threespine stickleback males Gasterosteus aculeatus, whose attractiveness to females was known, to either clear or algal‐turbid water, nest abandonment was more common in clear water, and it was usually the unattractive male that abandoned his nest. In turbid water, on the other hand, nest abandonments were less common and when they occurred, the probability increased that the attractive male abandoned his nest, and that the unattractive male subsequently occupied it. This change in the composition of nesting males increased the mating success of unattractive males. Thus, our results reveal a new mechanism through which habitat deterioration can influence sexual selection, by altering success in the competition for a resource critical in mate attraction, a territory with a nest in this case. This could be a common mechanism, considering the prevalence of resource competition in mate choice systems. On a broader level, our results emphasise the importance of considering the impact of environmental changes on the outcome of resource competition when investigating the influence that environmental disturbances have on the operation of sexual selection and thereby on evolutionary processes and population dynamics.

Assortative mating, sexual selection, and their consequences for gene flow inLittorina

When divergent populations are connected by gene flow, the establishment of complete reproductive isolation usually requires the joint action of multiple barrier effects. One example where multiple barrier effects are coupled consists of a single trait that is under divergent natural selection and also mediates assortative mating. Such multiple-effect traits can strongly reduce gene flow. However, there are few cases where patterns of assortative mating have been described quantitatively and their impact on gene flow has been determined. Two ecotypes of the coastal marine snail, Littorina saxatilis, occur in North Atlantic rocky-shore habitats dominated by either crab predation or wave action. There is evidence for divergent natural selection acting on size, and size-assortative mating has previously been documented. Here, we analyze the mating pattern in L.saxatilis with respect to size in intensively sampled transects across boundaries between the habitats. We show that the mating pattern is mostly conserved between ecotypes and that it generates both assortment and directional sexual selection for small male size. Using simulations, we show that the mating pattern can contribute to reproductive isolation between ecotypes but the barrier to gene flow is likely strengthened more by sexual selection than by assortment.

Sexual selection on size and shape in Japanese beetles (Popillia japonica)

AbstractThe mobility hypothesis argues that species in which males compete for mates in scrambles often exhibit female-biased size dimorphism because smaller male body size should increase male mobility and success in searching for mates. Sexual dimorphism can be further exaggerated if fecundity or sexual selection concurrently selects for larger female size. Scramble competition can select for trait characteristics that optimize locomotion; for example, long and slender wings should be favored if aerial speed is important to mating success. I tested these predictions in the scrambling Japanese beetle (Popillia japonica), a female-biased size dimorphic insect pest that is invasive to North America. Multivariate selection analyses support the prediction that smaller body size and larger wings in males benefit their mating success. My analyses also revealed significant selection for larger wings in females but, contrary to prediction, direct sexual selection favors smaller body size in females. These results support the mobility hypothesis and partially explain the evolution of female-biased size dimorphism in this species. Sexual selection favored rounder bodies in females and more tapered bodies in males, whereas, in both sexes, the effect of wing shape appears less important to fitness than wing size.

Warm developmental temperatures induce non‐adaptive plasticity in the intrasexually selected colouration of a dragonfly

1. When the breeding environment fluctuates across generations, reproductive traits may evolve plasticity that optimises the balance between survival and mating success for the prevailing environment.2. For sexually selected colouration, this balance can depend on environmental temperatures. Accordingly, breeding colouration often co‐varies with temperature through space and time. However, whether such traits exhibit plasticity in response to environmental temperatures is poorly understood.3. In the present study, a dragonfly (Pachydiplax longipennis) was reared under ambient or experimentally warmed conditions and tested for plasticity in its intrasexually selected wing colouration. Although wing colouration improves male territorial success, these advantages are smaller under warmer conditions than cooler conditions. It was therefore predicted that males reared under the ambient thermal conditions of the study site (Cleveland, Ohio) would develop more wing colouration than those reared under experimentally warmed conditions.4. Contrary to this prediction, males reared in warm larval temperatures produced more wing colouration. Thus, although the secondary sexual colouration of this species displays some thermal plasticity, it does not appear to be adaptive relative to the known thermal variation of intrasexual selection in this population.5. Given that the environment often determines the strength and direction of sexual selection, future studies should consider the potential for non‐adaptive, and even maladaptive, developmental plasticity in the sexually selected traits of insects.

Predator‐induced maternal and paternal effects independently alter sexual selection

Parental experience alters survival-related phenotypes of offspring in both adaptive and nonadaptive ways, yielding rapid inter- and transgenerational fitness effects. Yet, fitness comprises survival and reproduction, and parental effects on mating decisions could alter the strength and direction of sexual selection, affecting long-term evolutionary trajectories. We used a full factorial design in which threespine stickleback (Gasterosteus aculeatus) mothers, fathers, both, or neither were exposed to a model predator at developmentally appropriate times to test for predator-induced maternal, paternal, and joint parental effects on daughters' mating behavior. We tested the responsiveness, preferences, and mate choices of adult daughters in no-choice trials with wild-caught males who had varied sexual signals. Maternal and paternal predator exposure independently yielded daughters who preferred males who were intermediate in conspicuousness (with duller nuptial coloration and who courted less vigorously), relaxing the typical preference for the most conspicuous males. The combined effects of maternal and paternal predator exposure were not cumulative; when both parents were predator exposed, single-parent effects on mate preferences were reversed. Thus, we cannot assume that maternal and paternal effects additively combine to produce "parental" effects. Further, joint parental predator exposure yielded daughters who were three times less likely to mate at all. Stress-induced intergenerational parental effects on reproductive decisions such as those observed here may potentiate rapid transgenerational responses to novel and changing mating environments.

A multivariate analysis of women's mating strategies and sexual selection on men's facial morphology.

The strength and direction of sexual selection via female choice on masculine facial traits in men is a paradox in human mate choice research. While masculinity may communicate benefits to women and offspring directly (i.e. resources) or indirectly (i.e. health), masculine men may be costly as long-term partners owing to lower paternal investment. Mating strategy theory suggests women's preferences for masculine traits are strongest when the costs associated with masculinity are reduced. This study takes a multivariate approach to testing whether women's mate preferences are context-dependent. Women (n = 919) rated attractiveness when considering long-term and short-term relationships for male faces varying in beardedness (clean-shaven and full beards) and facial masculinity (30% and 60% feminized, unmanipulated, 30% and 60% masculinized). Participants then completed scales measuring pathogen, sexual and moral disgust, disgust towards ectoparasites, reproductive ambition, self-perceived mate value and the facial hair in partners and fathers. In contrast to past research, we found no associations between pathogen disgust, self-perceived mate value or reproductive ambition and facial masculinity preferences. However, we found a significant positive association between moral disgust and preferences for masculine faces and bearded faces. Preferences for beards were lower among women with higher ectoparasite disgust, providing evidence for ectoparasite avoidance hypothesis. However, women reporting higher pathogen disgust gave higher attractiveness ratings for bearded faces than women reporting lower pathogen disgust, providing support for parasite-stress theories of sexual selection and mate choice. Preferences for beards were also highest among single and married women with the strongest reproductive ambition. Overall, our results reflect mixed associations between individual differences in mating strategies and women's mate preferences for masculine facial traits.