Sex-specific overdominance at the maturation vgll3 gene for reproductive fitness in wild Atlantic salmon.

Linking reproductive fitness with adaptive traits at the genomic level can shed light on the mechanisms that produce and maintain sex-specific selection. Here, we construct a multigenerational pedigree to investigate sex-specific selection on a maturation gene, vgll3, in a wild Atlantic salmon population. The vgll3 locus is responsible for ~40% of the variation in maturation (sea age at first reproduction). Genetic parentage analysis was conducted on 18,265 juveniles (parr) and 685 adults collected at the same spawning ground over eight consecutive years. A high proportion of females (26%) were iteroparous and reproduced two to four times in their lifetime. A smaller proportion of males (9%) spawned at least twice in their lifetime. Sex-specific patterns of reproductive fitness were related to vgll3 genotype. Females showed a pattern of overdominance where vgll3*EL genotypes had three-fold more total offspring than homozygous females. In contrast, males demonstrated that late-maturing vgll3*LL individuals had two-fold more offspring than either vgll3*EE or vgll3*EL males. Taken together, these data suggest that balancing selection in females contributes to the maintenance of variation at this locus via increased fitness of iteroparous vgll3*EL females. This study demonstrates the utility of multigenerational pedigrees for uncovering complex patterns of reproduction, sex-specific selection and the maintenance of genetic variation.

Lateralised courtship behaviour and its impact on mating success in Ostrinia furnacalis (Lepidoptera: Crambidae).

Lateralisation is a well-established phenomenon observed in an increasing number of insect species. This study aims to obtain basic details on lateralisation in courtship and mating behaviour in Ostrinia furnacalis, the Asian corn borer. We conducted laboratory investigations to observe lateralisation in courtship and mating behaviours in adult O. furnacalis. Our goal was also to detect lateralised mating behaviour variations during sexual interactions and to elucidate how these variances might influence the mating success of males. Our findings reveal two distinct lateralised traits: male approaches from the right or left side of the female and the direction of male turning displays. Specifically, males approaching females from their right side predominantly exhibited left-biased 180° turning displays, while males approaching females from the left-side primarily displayed right-biased 180° turning displays. Notably, left-biased males, executing a 180° turn for end-to-end genital contact, initiated copulation with fewer attempts and began copulation earlier than their right-biased approaches with left-biased 180° turning displays. Furthermore, mating success was higher when males subsequently approached the right side of females during sexual encounters. Left-biased 180° turning males exhibited a higher number of successful mating interactions. These observations provide the first report on lateralisation in the reproductive behaviour of O. furnacalis under controlled laboratory conditions and hold promise for establishing reliable benchmarks for assessing and monitoring the quality of mass-produced individuals in pest control efforts.

Personality traits differentially affect components of reproductive success in a Neotropical poison frog.

Individual reproductive success has several components, including the acquisition of mating partners, offspring production, and offspring survival until adulthood. While the effects of certain personality traits-such as boldness or aggressiveness-on single components of reproductive success are well studied, we know little about the composite and multifaceted effects behavioural traits can have on all the aspects of reproductive success. Behavioural traits positively linked to one component of reproductive success might not be beneficial for other components, and these effects may differ between sexes. We investigated the influence of boldness, aggressiveness, and exploration on the number of mating partners, mating events, and offspring surviving until adulthood in males and females of the Neotropical poison frog Allobates femoralis. Behavioural traits had different-even opposite-effects on distinct components of reproductive success in both males and females. For example, males who displayed high levels of aggressiveness and exploration (or low levels of aggressiveness and exploration) managed to attract high number of mating partners, while males with low levels of boldness, low levels of aggressiveness, and high levels of exploration had the most offspring surviving until adulthood. Our results therefore suggest correlational selection favouring particular combinations of behavioural traits.

Trade-off between pre and post-copulatory traits depends on locomotor activity in male Tribolium castaneum beetles.

Locomotor performance is an indicator of dynamic exercise; thus, it is a central trait in many animal behaviours. Although higher locomotor endurance may increase male reproductive success (e.g., in mate searching and male-male contests), investment in other male reproductive traits (e.g., male attractiveness and sperm competition) may be decreased through energy consumption due to higher activity levels. Here, I investigated male attractiveness, mating success, and paternity success using males of the red flour beetle Tribolium castaneum selected for higher (H) and lower (L) locomotor endurance. Although there was no difference in male attractiveness between the selection regimes, H males had significantly higher mating success than L males. Conversely, L males had significantly higher paternity success than H males. Therefore, there was a trade-off between mating success and paternity success among the selection regimes, suggesting that locomotor endurance affects male reproduction in T. castaneum, and individual variation of locomotor endurance may be maintained within a population.

Adaptive function of duodichogamy: Why do chestnut trees have two pollen emission phases?

PREMISE: Intersexual mating facilitation in flowering plants has been largely underexplored. Duodichogamy is a rare flowering system in which individual plants flower in the sequence male-female-male. We studied the adaptive advantages of this flowering system using chestnuts (Castanea spp., Fagaceae) as models. These insect-pollinated trees produce many unisexual male catkins responsible for a first staminate phase and a few bisexual catkins responsible for a second staminate phase. We hypothesized that duodichogamy increases female mating success by facilitating pollen deposition on stigmas of the rewardless female flowers through their proximity with attractive male flowers responsible for the minor staminate phase. METHODS: We monitored insect visits to 11 chestnut trees during the entire flowering period and explored reproductive traits of all known duodichogamous species using published evidence. RESULTS: In chestnuts, insects visited trees more frequently during the first staminate phase but visited female flowers more frequently during the second staminate phase. All 21 animal-pollinated duodichogamous species identified are mass-flowering woody plants at high risk of self-pollination. In 20 of 21 cases, gynoecia (female flower parts) are located close to androecia (male flower parts), typically those responsible for the second minor staminate phase, whereas androecia are often distant from gynoecia. CONCLUSIONS: Our results suggest that duodichogamy increases female mating success by facilitating pollen deposition on stigmas by means of the attractiveness of the associated male flowers while effectively limiting self-pollination.

Conflicting constraints on male mating success shape reward size in pollen-rewarding plants.

PREMISE: Pollen-rewarding plants face two conflicting constraints: They must prevent consumptive emasculation while remaining attractive to pollen-collecting visitors. Small pollen packages (the quantity of pollen available in a single visit) may discourage visitors from grooming (reducing consumptive loss) but may also decrease a plant's attractiveness to pollen-collecting visitors. What package size best balances these two constraints? METHODS: We modeled the joint effects of pollinators' grooming behaviors and package size preferences on the optimal package size (i.e., the size that maximizes pollen donation). We then used this model to examine Darwin's conjecture that selection should favor increased pollen production in pollen-rewarding plants. RESULTS: When package size preferences are weak, minimizing package size reduces grooming losses and should be favored (as in previous theoretical studies). Stronger preferences select for larger packages despite the associated increase to grooming loss because loss associated with nonremoval of smaller packages is even greater. Total pollen donation increases with production (as Darwin suggested). However, if floral visitation declines or packages size preference increases with overall pollen availability, the fraction of pollen donated may decline as per-plant pollen production increases. Hence, increasing production may result in diminishing returns. CONCLUSIONS: Pollen-rewarding plants can balance conflicting constraints on pollen donation by producing intermediate-sized pollen packages. Strictly pollen-rewarding plants may have responded to past selection to produce more pollen in total, but diminishing returns may limit the strength of that selection.

Low and high temperatures decrease the mating success of an egg parasitoid and the proportion of females in the population.

Temperature influences all aspects of insect physiology and behaviour, including reproduction. Adverse temperatures can decrease mating success and sperm transfer, leading to increased sex ratio (more males) in populations of haplodiploid organisms. We tested the effect of five temperatures on the reproduction of the egg parasitoid Anaphes listronoti. Temperatures above and below 24.5°C decreased mating success by 30%-80%. Mating failures can arise from lack of encounters between sexes, absence of courting by the male, or the female refusing to mate. Both courtship and copulation duration decreased with increasing temperature. For mated females, there was no effect of mating temperature on offspring number and sex ratio. However, the increased number of virgin females at adverse temperatures did modify the simulated population sex ratio of the next generation, which increased from 0.2 at 24.5°C to 0.4, 0.5, 0.4 and 0.8 at 15.7°C, 20°C and 30°C and 35°C, respectively. The effect of temperature on courtship and copulation success of A. listronoti could lead to a decrease of the number of females in the population.

Fitness Implications of Nonlethal Injuries in Scorpions: Females, but Not Males, Pay Reproductive Costs.

AbstractThe ability to detach a body part in response to a predation attempt is known as autotomy, and it is perhaps the most intensively studied form of nonlethal injury in animals. Although autotomy enhances survival, it may impose reproductive costs on both males and females. We experimentally investigated how autotomy affects the reproductive success of males and females of a scorpion species. Individuals of Ananteris balzani autotomize the last abdominal segments (the tail), losing the anus and leading to lifelong constipation, since regeneration does not occur. Although the male tail is used during courtship and sperm transfer, autotomy has no effect on male mating success. The combined effect of increased mortality and reduced fecundity resulted in autotomized females producing nearly 35% fewer offspring than intact females. In conclusion, the negative effects of tail autotomy are clearly sex dependent, probably because the factors that influence reproductive success in males and females are markedly different.

Social network position experiences more variable selection than weaponry in wild subpopulations of forked fungus beetles.

The phenotypic expression and fitness consequences of behaviours that are exhibited during social interactions are especially sensitive to their local social context. This context-dependence is expected to generate more variation in the sign and magnitude of selection on social behaviour than that experienced by static characters like morphology. Relatively few studies, however, have examined selection on behavioural traits in multiple populations. We estimated sexual selection in the wild to determine if the strength and form of selection on social phenotypes is more variable than that on morphology. We compared selection gradients on social network position, body size, and weaponry of male forked fungus beetles Bolitotherus cornutus as they influenced mating success across nine natural subpopulations. Male horn length consistently experienced positive sexual selection. However, the sign and magnitude of selection on individual measures of network centrality (strength and betweenness) differed significantly among subpopulations. Moreover, selection on social behaviours occurred at a local scale ('soft selection'), whereas selection on horn length occurred at the metapopulation scale ('hard selection'). These results indicate that an individual with a given social phenotype could experience different fitness consequences depending on the network it occupies. While individuals seem to be unable to escape the fitness effects of their morphology, they may have the potential to mediate the pressures of selection on behavioural phenotypes by moving among subpopulations or altering social connections within a network.

An analysis of mating biases in trees.

Assortative mating is a deviation from random mating based on phenotypic similarity. As it is much better studied in animals than in plants, we investigate for trees whether kinship of realized mating pairs deviates from what is expected from the set of potential mates and use this information to infer mating biases that may result from kin recognition and/or assortative mating. Our analysis covers 20 species of trees for which microsatellite data is available for adult populations (potential mates) as well as seed arrays. We test whether mean relatedness of observed mating pairs deviates from null expectations that only take pollen dispersal distances into account (estimated from the same data set). This allows the identification of elevated as well as reduced kinship among realized mating pairs, indicative of positive and negative assortative mating, respectively. The test is also able to distinguish elevated biparental inbreeding that occurs solely as a result of related pairs growing closer to each other from further assortativeness. Assortative mating in trees appears potentially common but not ubiquitous: nine data sets show mating bias with elevated inbreeding, nine do not deviate significantly from the null expectation, and two show mating bias with reduced inbreeding. While our data sets lack direct information on phenology, our investigation of the phenological literature for each species identifies flowering phenology as a potential driver of positive assortative mating (leading to elevated inbreeding) in trees. Since active kin recognition provides an alternative hypothesis for these patterns, we encourage further investigations on the processes and traits that influence mating patterns in trees.

Time spent in distinct life history stages has sex-specific effects on reproductive fitness in wild Atlantic salmon.

In species with complex life cycles, life history theory predicts that fitness is affected by conditions encountered in previous life history stages. Here, we use a 4-year pedigree to investigate if time spent in two distinct life history stages has sex-specific reproductive fitness consequences in anadromous Atlantic salmon (Salmo salar). We determined the amount of years spent in fresh water as juveniles (freshwater age, FW, measured in years), and years spent in the marine environment as adults (sea age, SW, measured in sea winters) on 264 sexually mature adults collected on a river spawning ground. We then estimated reproductive fitness as the number of offspring (reproductive success) and the number of mates (mating success) using genetic parentage analysis (>5,000 offspring). Sea age is significantly and positively correlated with reproductive and mating success of both sexes whereby older and larger individuals gained the highest reproductive fitness benefits (females: 62.2% increase in offspring/SW and 34.8% increase in mate number/SW; males: 201.9% offspring/SW and 60.3% mates/SW). Younger freshwater age was significantly related to older sea age and thus increased reproductive fitness, but only among females (females: -33.9% offspring/FW and -32.4% mates/FW). This result implies that females can obtain higher reproductive fitness by transitioning to the marine environment earlier. In contrast, male mating and reproductive success was unaffected by freshwater age and more males returned at a younger age than females despite the reproductive fitness advantage of later sea age maturation. Our results show that the timing of transitions between juvenile and adult phases has a sex-specific consequence on female reproductive fitness, demonstrating a life history trade-off between maturation and reproduction in wild Atlantic salmon.

No evidence that Y-chromosome differentiation affects male fitness in a Swiss population of common frogs.

The canonical model of sex-chromosome evolution assigns a key role to sexually antagonistic (SA) genes on the arrest of recombination and ensuing degeneration of Y chromosomes. This assumption cannot be tested in organisms with highly differentiated sex chromosomes, such as mammals or birds, owing to the lack of polymorphism. Fixation of SA alleles, furthermore, might be the consequence rather than the cause of recombination arrest. Here we focus on a population of common frogs (Rana temporaria) where XY males with genetically differentiated Y chromosomes (nonrecombinant Y haplotypes) coexist with both XY° males with proto-Y chromosomes (only differentiated from X chromosomes in the immediate vicinity of the candidate sex-determining locus Dmrt1) and XX males with undifferentiated sex chromosomes (genetically identical to XX females). Our study finds no effect of sex-chromosome differentiation on male phenotype, mating success or fathering success. Our conclusions rejoin genomic studies that found no differences in gene expression between XY, XY° and XX males. Sexual dimorphism in common frogs might result more from the differential expression of autosomal genes than from sex-linked SA genes. Among-male variance in sex-chromosome differentiation seems better explained by a polymorphism in the penetrance of alleles at the sex locus, resulting in variable levels of sex reversal (and thus of X-Y recombination in XY females), independent of sex-linked SA genes.

Individual and synergistic effects of male external genital traits in sexual selection.

Male genital traits exhibit extraordinary interspecific phenotypic variation. This remarkable and general evolutionary trend is widely considered to be the result of sexual selection. However, we still do not have a good understanding of whether or how individual genital traits function in different competitive arenas (episodes of sexual selection), or how different genital traits may interact to influence competitive outcomes. Here, we use an experimental approach based on high-precision laser phenotypic engineering to address these outstanding questions, focusing on three distinct sets of micron-scale external (nonintromittent) genital spines in male Drosophila kikkawai Burla (Diptera: Drosophilidae). Elimination of the large pair of spines on the male secondary claspers sharply reduced male ability to copulate, yet elimination of the other sets of spines on the primary and secondary claspers had no significant effects on copulation probability. Intriguingly, both the large spines on the secondary claspers and the cluster of spines on the primary claspers were found to independently promote male competitive fertilization success. Moreover, when large and small secondary clasper spines were simultaneously shortened in individual males, these males suffered greater reductions in fertilization success relative to males whose traits were altered individually, providing evidence for synergistic effects of external genital traits on fertilization success. Overall, the results are significant in demonstrating that a given genital trait (the large spines on the secondary claspers) can function in different episodes of sexual selection, and distinct genital traits may interact in sexual selection. The results offer an important contribution to evolutionary biology by demonstrating an understudied selective mechanism, operating via subtle trait interactions in a post-insemination context, by which genital traits may be co-evolving.

Mating Delay Reduces Reproductive Performance but not Longevity in a Monandrous Moth.

Age at mating is one of the most important factors that affect mating success and reproductive fitness in insects. The present study investigated how the age of the two sexes at mating determined mating success, reproductive fitness and longevity in Phauda flammans (Walker) (Lepidoptera: Phaudidae), a serious pest of Ficus spp. trees in South and Southeast Asia. The study may provide basic knowledge for the development of mating disruption programs using sex pheromones to control this pest. The species is monandrous and its adults live for only 4-5 d. We show that delayed mating significantly lowered mating success in both sexes, with males being more severely affected than females. Mating delay also reduced reproductive outputs of both sexes but females were more negatively affected than males. We did not find any effect of delayed mating on longevity of either sex. Our findings suggest that mating disruption with sex pheromones can be an effective method to delay mating in P. flammans, reducing reproductive success and thus limit population growth.

Male competition and the evolution of mating and life-history traits in experimental populations of Aedes aegypti.

Aedes aegypti is an important disease vector and a major target of reproductive control efforts. We manipulated the opportunity for sexual selection in populations of Ae. aegypti by controlling the number of males competing for a single female. Populations exposed to higher levels of male competition rapidly evolved higher male competitive mating success relative to populations evolved in the absence of competition, with an evolutionary response visible after only five generations. We also detected correlated evolution in other important mating and life-history traits, such as acoustic signalling, fecundity and body size. Our results indicate that there is ample segregating variation for determinants of male mating competitiveness in wild populations and that increased male mating success trades-off with other important life-history traits. The mating conditions imposed on laboratory-reared mosquitoes are likely a significant determinant of male mating success in populations destined for release.

Field estimates of fitness costs of the pace-of-life in an endangered damselfly.

Theory predicts that within-population differences in the pace-of-life can lead to cohort splitting and produce marked intraspecific variation in body size. Although many studies showed that body size is positively correlated with fitness, many argue that selection for the larger body is counterbalanced by opposing physiological and ecological selective mechanisms that favour smaller body. When a population split into cohorts with different paces of life (slow or fast cohort), one would expect to detect the fitness-size relationship among and within cohorts, that is, (a) slower-developing cohort has larger body size and higher fitness than faster-developing cohort, and (b) larger individuals within each cohort show higher fitness than smaller individuals. Here, we test these hypotheses in capture-mark-recapture field surveys that assess body size, lifespan, survival and lifetime mating success in two consecutive generations of a partially bivoltine aquatic insect, Coenagrion mercuriale, where the spring cohort is slower-developing than the autumn cohort. As expected, body size was larger in the slow-developing cohort, which is consistent with the temperature-size rule and also with the duration of development. Body size seasonal variation was greater in slow-developing cohort most likely because of the higher variation in age at maturity. Concordant with theory, survival probability, lifespan and lifetime mating success were higher in the slow-developing cohort. Moreover, individual body size was positively correlated with survival and mating success in both cohorts. Our study confirms the fitness costs of fast pace-of-life and the benefits of larger body size to adult fitness.

Costs and benefits of giant sperm and sperm storage organs in Drosophila melanogaster.

In Drosophila, long sperm are favoured in sperm competition based on the length of the female's primary sperm storage organ, the seminal receptacle (SR). This sperm-SR interaction, together with a genetic correlation between the traits, suggests that the coevolution of exaggerated sperm and SR lengths may be driven by Fisherian runaway selection. Here, we explore the costs and benefits of long sperm and SR genotypes, both in the sex that carries them and in the sex that does not. We measured male and female fitness in inbred lines of Drosophila melanogaster derived from four populations previously selected for long sperm, short sperm, long SRs or short SRs. We specifically asked: What are the costs and benefits of long sperm in males and long SRs in females? Furthermore, do genotypes that generate long sperm in males or long SRs in females impose a fitness cost on the opposite sex? Answers to these questions will address whether long sperm are an honest indicator of male fitness, male post-copulatory success is associated with male precopulatory success, female choice benefits females or is costly, and intragenomic conflict could influence evolution of these traits. We found that both sexes have increased longevity in long sperm and long SR genotypes. Males, but not females, from long SR lines had higher fecundity. Our results suggest that sperm-SR coevolution is facilitated by both increased viability and indirect benefits of long sperm and SRs in both sexes.

Heat-hardening effects on mating success at high temperature in Drosophila melanogaster.

Reproduction is strongly influenced by environmental temperature in insects. At high temperature, mating success could be influenced not only by basal (non-inducible) thermotolerance but also by inducible plastic responses. Here, mating success at high temperature was tested in flies carrying contrasting genotypes of heat resistance in Drosophila melanogaster. The possible heat-hardening effect was tested. Mating success did not differ between heat-resistant and heat-sensitive genotypes when tested both at high (33 °C) and benign (25 °C) temperature, independently of the heat-hardening status. Importantly, heat-hardening pre-treatment increased in a 70% the number of matings at 33 °C in a mass-mating experiment. Further, mating latency at 33 °C was shorter with heat hardening than without it in single-pair assays Heat-hardening had previously been showed to improve short-term thermotolerance in many organisms including Drosophila, and the present results show that heat hardening also improve mating success at elevated temperature. Previous exposures to a mild heat stress improve short-term mating success as a plastic response of ecological relevance. Such heat-hardening effects on mating success should be relevant for predicting potential evolutionary responses to any possible current scenery of global warming, as well as in sterile insect release programs for pest control in elevated temperature environments.

Evidence that fertility trades off with early offspring fitness as males age.

Models of ageing predict that sperm function and fertility should decline with age as sperm are exposed to free radical damage and mutation accumulation. However, theory also suggests that mating with older males should be beneficial for females because survival to old age is a demonstration of a male's high genetic and/or phenotypic quality. Consequently, declines in sperm fitness may be offset by indirect fitness benefits exhibited in offspring. While numerous studies have investigated age-based declines in male fertility, none has taken the integrated approach of studying age-based effects on both male fertility and offspring fitness. Here, using a cohort-based longitudinal study of zebrafish (Danio rerio), we report a decline in male mating success and fertility with male age but also compensating indirect benefits. Using in vitro fertilization, we show that offspring from older males exhibit superior early survival compared to those from their youngest counterparts. These findings suggest that the high offspring fitness observed for the subset of males that survive to an old age (approx. 51% in this study) may represent compensating benefits for declining fertility with age, thus challenging widely held views about the fitness costs of mating with older males.

Commentary on Kehl et al. "Young male mating success is associated with sperm number but not with male sex pheromone titres": Unnatural experimental conditions inflate the importance of male courtship activity on mating success in a butterfly.

Over the last years, several studies suggested that male courtship activity is more important than female preference for male secondary sexual traits in determining male mating success in the butterfly Bicyclus anynana. We use Kehl et al. (Front Zool 12, 2015)'s study and related publications, to highlight three methodological and conceptual aspects of laboratory experiments that distort the social environment compared to natural conditions. We argue that such experimental biases prevent the expression of female mate choice and artificially inflate the role of male activity in determining mating success. We really want to stress that any work performed in laboratory conditions using extreme cage densities or sizes impedes female mate choice and promotes male-male competition when sexual conflict occurs about mating decisions. Hence, such studies, and the derived conclusions, are only applicable to ecologically-irrelevant conditions and cannot be extrapolated to more natural laboratory or field conditions. Our concerns may be relevant to many behavioural studies quantifying sexual selection across taxa. This commentary adds to the increasing scientific awareness that: i) mating outcome is, across taxa, the result of a sexual conflict whose outcome is under female, and not male, control; ii) the social environment used to quantify mating success is of utmost importance to produce reliable estimates of the strength and the direction of sexual selection on sexually-selected traits, as they evolve in nature.