SEXUAL SELECTION AGAINST HYBRIDS BETWEEN SYMPATRIC STICKLEBACK SPECIES: EVIDENCE FROM A FIELD EXPERIMENT

Sexual selection against viable, fertile hybrids may contribute to reproductive isolation between recently diverged species. If so, then sexual selection may be implicated in the speciation process. Laboratory measures of the mating success of hybrids may underestimate the amount of sexual selection against them if selection pressures are habitat specific. Male F₁ hybrids between sympatric benthic and limnetic sticklebacks (Gasterosteus aculeatus complex) do not suffer a mating disadvantage when tested in the laboratory. However, in the wild males choose different microhabitats and parental females tend to be found in the same habitats as conspecific males. This sets up the opportunity for sexual selection against male hybrids because they must compete with parental males for access to parental females. To test for sexual selection against adult F₁ hybrid males, we examined their mating success in enclosures in their preferred habitat (open, unvegetated substrate) where limnetic males and females also predominate. We found significantly reduced mating success in F₁ hybrid males compared with limnetic males. Thus, sexual selection, like other mechanisms of postzygotic isolation between young sister species, may be stronger in a wild setting than in the laboratory because of habitat-specific selection pressures. Our results are consistent with, but do not confirm, a role for sexual selection in stickleback speciation.     

Strong sexual selection in males against a mutation load that reduces offspring production in seed beetles

Theory predicts that sexual reproduction can increase population viability relative to asexual reproduction by allowing sexual selection in males to remove deleterious mutations from the population without large demographic costs. This requires that selection acts more strongly in males than females and that mutations affecting male reproductive success have pleiotropic effects on population productivity, but empirical support for these assumptions is mixed. We used the seed beetle Callosobruchus maculatus to implement a three‐generation breeding design where we induced mutations via ionizing radiation (IR) in the F₀ generation and measured mutational effects (relative to nonirradiated controls) on an estimate of population productivity in the F₁ and effects on sex‐specific competitive lifetime reproductive success (LRS) in the F₂. Regardless of whether mutations were induced via F₀ males or females, they had strong negative effects on male LRS, but a nonsignificant influence on female LRS, suggesting that selection is more efficient in removing deleterious alleles in males. Moreover, mutations had seemingly shared effects on population productivity and competitive LRS in both sexes. Thus, our results lend support to the hypothesis that strong sexual selection on males can act to remove the mutation load on population viability, thereby offering a benefit to sexual reproduction.     

Genetic evidence for the mating system and reproductive success of black sea bream (Acanthopagrus schlegelii)

Understanding the mating system and reproductive success of a species provides evidence for sexual selection. We examined the mating system and the reproductive success of captive adult black sea bream (Acanthopagrus schlegelii), using parentage assignment based on two microsatellites multiplex PCR systems, with 91.5% accuracy in a mixed family (29 sires, 25 dams, and 200 offspring). Based on the parentage result, we found that 93.1% of males and 100% of females participated in reproduction. A total of 79% of males and 92% of females mated with multiple partners (only 1 sire and 1 dam were monogamous), indicating that polygynandry best described the genetic mating system of black sea bream. For males, maximizing the reproductive success by multiple mating was accorded with the sexual selection theory while the material benefits hypothesis may contribute to explain the multiple mating for females. For both sexes, there was a significant correlation between mating success and reproductive success and the variance in reproductive success of males was higher than females. Variation in mating success is the greatest determinant to variation in reproductive success when the relationship is strongly positive. The opportunity for sexual selection of males was twice that of females, as well as the higher slope of the Bateman curve in males suggested that the intensity of intrasexual selection of males was higher than females. Thus, male–male competition would lead to the greater variation of mating success for males, which caused greater variation in reproductive success in males. The effective population number of breeders (N_b) was 33, and the N_b/N ratio was 0.61, slightly higher than the general ratio in polygynandrous fish populations which possibly because most individuals mated and had offspring with a low variance. The relatively high N_b contributes to the maintenance of genetic diversity in farmed black sea bream populations.     

OPERATIONAL SEX RATIO BUT NOT DENSITY AFFECTS SEXUAL SELECTION IN A FISH

The operational sex ratio (OSR) and density are considered important factors affecting the strength of sexual selection. Although there is increasing evidence that OSR and density affect the potential for sexual selection, few studies have addressed whether this is realized in phenotypic selection and how the two factors interact. We manipulated OSR (three levels) and male density (two levels) in 36 experimental breeding populations of Gobiusculus flavescens—a fish with paternal care. We measured mating competition behavior, the opportunity for selection (I), and selection on four morphological traits in males. We found sexual selection on two male traits, with the strongest selection being 20% of I. As predicted from OSR theory, increasing female scarcity caused males to become more competitive, concomitant with an increase in I and selection on morphological traits. Model simulations of I based on random mating (I_min) and maximum mate monopolization (I_max) demonstrated that the potential for sexual selection was close to its theoretical maximum across the range of OSRs. However, male density and its interaction with the OSR did not affect sexual selection. We argue that a multifaceted approach, combining mating behavior and selection analyses, can help us to understand how ecological factors affect sexual selection.     

Sexual conflict and environmental change: trade-offs within and between the sexes during the evolution of desiccation resistance

Intralocus sexual conflict occurs when males and females experience sex-specific selection on a shared genome. With several notable exceptions, intralocus sexual conflict has been investigated in constant environments to which the study organisms have had an opportunity to adapt. However, a change in the environment can result in differential or even opposing selection pressures on males and females, creating sexual conflict. We used experimental evolution to explore the interaction between intralocus sexual conflict, sexual dimorphism and environmental variation in Drosophila melanogaster. Six populations were selected for adult desiccation resistance (D), with six matched control populations maintained in parallel (C). After 46 generations, the D populations had increased in survival time under arid conditions by 68% and in body weight by 20% compared to the C populations. The increase in size was the result of both extended development and faster growth rate of D juveniles. Adaptation to the stress came at a cost in terms of preadult viability and female fecundity. Because males are innately less tolerant of desiccation stress, very few D males survived desiccation-selection; while potentially a windfall for survivors, these conditions mean that most males’ fitness was determined posthumously. We conjectured that selection for early maturation and mating in males was in conflict with selection for survival and later reproduction in females. Consistent with this prediction, the sexes showed different patterns of age-specific desiccation resistance and resource acquisition, and there was a trend towards increasingly female-biased sexual size dimorphism. However, levels of desiccation resistance were unaffected, with D males and females increasing in parallel. Either there is a strong positive genetic correlation between the sexes that limits independent evolution of desiccation resistance, or fitness pay-offs from the strategy of riding out the stress bout are great enough to sustain concordant selection on the two sexes. We discuss the forces that mould fitness in males under a regimen where trade-offs between survival and reproduction may be considerable.     

Experimental evidence for accelerated adaptation to desiccation through sexual selection on males

The impact of sexual selection on the adaptive process remains unclear. On the one hand, sexual selection might hinder adaptation by favouring costly traits and preferences that reduce nonsexual fitness. On the other hand, condition dependence of success in sexual selection may accelerate adaptation. Here, we used replicate populations of Drosophila melanogaster to artificially select on male desiccation resistance while manipulating the opportunity for precopulatory sexual selection in a factorial design. Following five generations of artificial selection, we measured the desiccation resistance of males and females to test whether the addition of sexual selection accelerated adaptation. We found a significant interaction between the effects of natural selection and sexual selection: desiccation resistance was highest in populations where sexual selection was allowed to operate. Despite only selecting on males, we also found a correlated response in females. These results provide empirical support for the idea that sexual selection can accelerate the rate of adaptation.     

The large X‐effect on secondary sexual characters and the genetics of variation in sex comb tooth number in Drosophila subobscura

Genetic studies of secondary sexual traits provide insights into whether and how selection drove their divergence among populations, and these studies often focus on the fraction of variation attributable to genes on the X‐chromosome. However, such studies may sometimes misinterpret the amount of variation attributable to the X‐chromosome if using only simple reciprocal F₁ crosses, or they may presume sexual selection has affected the observed phenotypic variation. We examined the genetics of a secondary sexual trait, male sex comb size, in Drosophila subobscura. This species bears unusually large sex combs for its species group, and therefore, this trait may be a good candidate for having been affected by natural or sexual selection. We observed significant heritable variation in number of teeth of the distal sex comb across strains. While reciprocal F₁ crosses seemed to implicate a disproportionate X‐chromosome effect, further examination in the F₂ progeny showed that transgressive autosomal effects inflated the estimate of variation associated with the X‐chromosome in the F₁. Instead, the X‐chromosome appears to confer the smallest contribution of all major chromosomes to the observed phenotypic variation. Further, we failed to detect effects on copulation latency or duration associated with the observed phenotypic variation. Overall, this study presents an examination of the genetics underlying segregating phenotypic variation within species and illustrates two common pitfalls associated with some past studies of the genetic basis of secondary sexual traits.     

The opportunity for sexual selection: not mismeasured, just misunderstood

Evolutionary biologists have developed several indices, such as selection gradients (β) and the opportunity for sexual selection (I_s), to quantify the actual and/or potential strength of sexual selection acting in natural or experimental populations. In a recent paper, Klug et al. (J. Evol. Biol. 23 , 2010, 447) contend that selection gradients are the only legitimate metric for quantifying sexual selection. They argue that I_s and similar mating‐system‐based metrics provide unpredictable results, which may be uncorrelated with selection acting on a trait, and should therefore be abandoned. We find this view short‐sighted and argue that the choice of metric should be governed by the research question at hand. We describe insights that measures such as the opportunity for selection can provide and also argue that Klug et al. have overstated the problems with this approach while glossing over similar issues with the interpretation of selection gradients. While no metric perfectly characterizes sexual selection in all circumstances, thoughtful application of existing measures has been and continues to be informative in evolutionary studies.     

Genome‐wide selection components analysis in a fish with male pregnancy

A major goal of evolutionary biology is to identify the genome‐level targets of natural and sexual selection. With the advent of next‐generation sequencing, whole‐genome selection components analysis provides a promising avenue in the search for loci affected by selection in nature. Here, we implement a genome‐wide selection components analysis in the sex role reversed Gulf pipefish, Syngnathus scovelli. Our approach involves a double‐digest restriction‐site associated DNA sequencing (ddRAD‐seq) technique, applied to adult females, nonpregnant males, pregnant males, and their offspring. An F_ST comparison of allele frequencies among these groups reveals 47 genomic regions putatively experiencing sexual selection, as well as 468 regions showing a signature of differential viability selection between males and females. A complementary likelihood ratio test identifies similar patterns in the data as the F_ST analysis. Sexual selection and viability selection both tend to favor the rare alleles in the population. Ultimately, we conclude that genome‐wide selection components analysis can be a useful tool to complement other approaches in the effort to pinpoint genome‐level targets of selection in the wild.     

Reproductive behaviour evolves rapidly when intralocus sexual conflict is removed

Background

Intralocus sexual conflict can inhibit the evolution of each sex towards its own fitness optimum. In a previous study, we confirmed this prediction through the experimental removal of female selection pressures in Drosophila melanogaster, achieved by limiting the expression of all major chromosomes to males. Compared to the control populations (C_1-4) where the genomes are exposed to selection in both sexes, the populations with male-limited genomes (ML_1-4) showed rapid increases in male fitness, whereas the fitness of females expressing ML-evolved chromosomes decreased [1].

Methodology/Principal Findings

Here we examine the behavioural phenotype underlying this sexual antagonism. We show that males expressing the ML genomes have a reduced courtship level but acquire the same number of matings. On the other hand, our data suggest that females expressing the ML genomes had reduced attractiveness, stimulating a lower rate of courtship from males. Moreover, females expressing ML genomes tend to display reduced yeast-feeding behaviour, which is probably linked to the reduction of their fecundity.

Conclusion/Significance

These results suggest that reproductive behaviour is shaped by opposing selection on males and females, and that loci influencing attractiveness and foraging were polymorphic for alleles with sexually antagonistic expression patterns prior to ML selection. Hence, intralocus sexual conflict appears to play a role in the evolution of a wide range of fitness-related traits and may be a powerful mechanism for the maintenance of genetic variation in fitness.     

Population Genomic Analyses Based on 1 Million SNPs in Commercial Egg Layers

Identifying signatures of selection can provide valuable insight about the genes or genomic regions that are or have been under selective pressure, which can lead to a better understanding of genotype-phenotype relationships. A common strategy for selection signature detection is to compare samples from several populations and search for genomic regions with outstanding genetic differentiation. Wright''s fixation index, F_ST, is a useful index for evaluation of genetic differentiation between populations. The aim of this study was to detect selective signatures between different chicken groups based on SNP-wise F_ST calculation. A total of 96 individuals of three commercial layer breeds and 14 non-commercial fancy breeds were genotyped with three different 600K SNP-chips. After filtering a total of 1 million SNPs were available for F_ST calculation. Averages of F_ST values were calculated for overlapping windows. Comparisons of these were then conducted between commercial egg layers and non-commercial fancy breeds, as well as between white egg layers and brown egg layers. Comparing non-commercial and commercial breeds resulted in the detection of 630 selective signatures, while 656 selective signatures were detected in the comparison between the commercial egg-layer breeds. Annotation of selection signature regions revealed various genes corresponding to productions traits, for which layer breeds were selected. Among them were NCOA1, SREBF2 and RALGAPA1 associated with reproductive traits, broodiness and egg production. Furthermore, several of the detected genes were associated with growth and carcass traits, including POMC, PRKAB2, SPP1, IGF2, CAPN1, TGFb2 and IGFBP2. Our approach demonstrates that including different populations with a specific breeding history can provide a unique opportunity for a better understanding of farm animal selection.     

The Opportunity for Post-Copulatory Sexual Selection in the Ectoparasitic Pea Crab,Dissodactylus primitivus (Brachyura: Pinnotheridae)

Pea crabs, Dissodactylus primitivus, inhabit multiple echinoid (heart urchin) hosts. Male and female crabs move among hosts in search for mates, and both sexes mate multiple times, creating opportunities for post-copulatory sexual selection. For such selection to occur, only a fraction of the males who succeed in mating can also succeed in siring progeny. Jossart et al. 2014 used 4 microsatellite loci to document parentage and mating frequencies of both sexes in D. primitivus. From these data we identified the mean and variance in female offspring numbers, as well as the proportions of the female population that were gravid and not bearing offspring. We next identified the proportions of the male population who had (1) mated and sired offspring, (2) mated but failed to sire offspring, and (3) failed to mate altogether. We used these results to estimate the opportunity for selection on males and females in terms of mate numbers and offspring numbers, and estimated the sex difference in the opportunity for selection (i.e., the opportunity for sexual selection) using both forms of data. We then partitioned the total variance in male fitness into pre- and post-copulatory components and identified the fraction of the total opportunity for selection occurring in each context. Our results show that the opportunity for selection on each sex was of similar magnitude (0.69–0.98), consistent with this polyandrogynous mating system. We also found that 37% of the total opportunity for sexual selection on males occurred within the context of post-copulatory sexual selection. However, the fraction of the total opportunity for selection that was due to sexual selection, estimated using both mate numbers and offspring numbers, was 9% and 23% respectively. Thus, we further reduced our estimate of the opportunity for post-copulatory sexual selection in D. primitivus to less than 10% of the total opportunity for selection (0.37 of 0.09 and 0.23 = 0.03 and 0.09). Our results provide the first estimate of the maximum possible strength of post-copulatory sexual selection in crustaceans using this approach.     

Spatial and temporal patterns of nest distribution influence sexual selection in a marine fish

In many species, the natural distribution of material resources important for reproduction can profoundly impact reproductive success among individuals and, hence, the opportunity and intensity of sexual selection. Here, we report on a field‐based experiment investigating the effects of nest aggregation on sexual selection in a fish, the sand goby Pomatoschistus minutus. We found that the distribution of potential nests (sparse versus aggregated nest treatments) affected patterns of nest colonization and reproductive success. Specifically, in the treatment with aggregated nesting resources, a greater proportion of nests remained unoccupied by sand goby males. Although the size of nesting males did not differ between treatments, eggs accumulated more rapidly when nests were sparsely distributed. We found that the opportunity for selection decreased over time with the accumulation of eggs in the nests in both the aggregated and sparse treatments. Moreover, the effect of male size on reproductive success was influenced by an interaction between nest distribution and time, with the selection gradient being highest right after nest colonization when nests were aggregated, while the opposite pattern was observed in the sparse nest treatment. Such findings highlight the vital role that environmental and social factors can play in determining the importance of male phenotypic traits (in this case, male size). More broadly, our results also underscore how the natural distribution of resources, both in space and time, can impact the strength of sexual selection acting on wild animal populations.     

Growth to sexual maturity of dwarf and nondwarf White Rock chickens divergently selected for juvenile body weight

Summary Growth from hatching to the onset of lay (sexual maturity) was studied in White Plymouth Rock pullets from lines selected for high (HN) and low (LN) 56-day body weight, their reciprocal F₁ crosses, an F₂ cross, and two dwarf populations originating from the HN and LN parental lines. The highest R²s for describing growth for all populations except HN were obtained when body weight was expressed relative to body weight at sexual maturity. Modes of inheritance differed depending on whether patterns of growth were expressed in a chronological time frame or on a physiological basis. Heterosis observed for age at sexual maturity and for body weight after the age when selection was made was not in evidence when ages and weights were expressed as a proportion of those at sexual maturity.This research was supported, in part, by BARD Project No. US-675-83C     

LIFETIME REPRODUCTIVE SUCCESS AND THE OPPORTUNITY FOR SELECTION IN A NONTERRITORIAL DAMSELFLY (ODONATA: COENAGRIONIDAE)

Major components of male and female lifetime reproductive success (LRS) were quantified for a damselfly that exhibits “scramble competition” for mates. The opportunity for selection on male reproduction was potentially 2.9 times that for females. Differential fertility/clutch and survivorship each accounted for about half of the total variation in female reproductive success. Variation in fertilization efficiency accounted for 7% of the total opportunity for selection on males. Although differences in survivorship and mating efficiency each contributed to about a third of the total opportunity for selection on male reproduction, both components appeared to be influenced by random factors. Survivorship was age-independent, and the mating distributions among males with equal mating opportunities were indistinguishable from those expected if matings were random with respect to male phenotype. Because the proportion of the standarized variance (I) in LRS that was attributed to sexual selection depended on the way the selective episodes were defined, the sample of individuals included in the partitioning analysis, and the degree of sexual selection on mated males that could be detected, my results caution against drawing conclusions about the dynamics of sexual selection on populations based on a superficial comparison of I values.     

THE GENETIC BASIS OF SEXUAL ISOLATION BETWEEN DROSOPHILA MELANOGASTER AND D. SIMULANS

The genetic analysis of sexual isolation between the closely-related species Drosophila melanogaster and Drosophila simulans involved two experiments with no-choice tests. The efficiency of sexual isolation was measured by the frequency of courtship initiation and interspecific mating. We first surveyed the variation in sexual isolation between D. melanogaster strains and D. simulans strains of different geographic origin. Then, to investigate variation in sexual isolation within strains, we made F₁ diallel sets of reciprocal crosses within strains of D. melanogaster and D. simulans. The F₁ diallel progeny of one sex were paired with the opposite sex of the other species. The first experiment showed significant differences in the frequency of interspecific mating between geographic strains. There were more matings between D. simulans females and D. melanogaster males than between D. melanogaster females and D. simulans males. The second experiment uncovered that the male genotypes in the D. melanogaster diallel significantly differed in interspecific mating frequency, but not in courtship initiation frequency. The female genotypes in the D. simulans diallel were not significantly different in courtship initiation and interspecific mating frequency. Genetic analysis reveals that in D. melanogaster males sexual isolation was not affected by either maternal cytoplasmic effects, sex-linked effects, or epistatic interaction. The main genetic components were directional dominance and overdominance. The F₁ males achieved more matings with D. simulans females than the inbred males. The genetic architecture of sexual isolation in D. melanogaster males argues for a history of weak or no selection for lower interspecific mating propensity. The behavioral causes of variation in sexual isolation between the two species are discussed.     

Genetic and Economic Analysis of a Targeted Marker-assisted Wheat Breeding Strategy

The advent of molecular markers as a tool to aid selection has provided plant breeders with the opportunity to rapidly deliver superior genetic solutions to problems in agricultural production systems. However, a major constraint to the implementation of marker-assisted selection (MAS) in pragmatic breeding programs in the past has been the perceived high relative cost of MAS compared to conventional phenotypic selection. In this paper, computer simulation was used to design a genetically effective and economically efficient marker-assisted breeding strategy aimed at a specific outcome. Under investigation was a strategy involving the integration of both restricted backcrossing and doubled haploid (DH) technology. The point at which molecular markers are applied in a selection strategy can be critical to the effectiveness and cost efficiency of that strategy. The application of molecular markers was considered at three phases in the strategy: allele enrichment in the BC₁F₁ population, gene selection at the haploid stage and the selection for recurrent parent background of DHs prior to field testing. Overall, incorporating MAS at all three stages was the most effective, in terms of delivering a high frequency of desired outcomes and at combining the selected favourable rust resistance, end use quality and grain yield alleles. However, when costs were included in the model the combination of MAS at the BC₁F₁ and haploid stage was identified as the optimal strategy. A detailed economic analysis showed that incorporation of marker selection at these two stages not only increased genetic gain over the phenotypic alternative but actually reduced the over all cost by 40%.     

Genetic analysis of male reproductive success in relation to density in the zebrafish, Danio rerio

Background

We used behavioural and genetic data to investigate the effects of density on male reproductive success in the zebrafish, Danio rerio. Based on previous measurements of aggression and courtship behaviour by territorial males, we predicted that they would sire more offspring than non-territorial males.

Results

Microsatellite analysis of paternity showed that at low densities territorial males had higher reproductive success than non-territorial males. However, at high density territorial males were no more successful than non-territorials and the sex difference in the opportunity for sexual selection, based on the parameter I _mates, was low.

Conclusion

Male zebrafish exhibit two distinct mating tactics; territoriality and active pursuit of females. Male reproductive success is density dependent and the opportunity for sexual selection appears to be weak in this species.     

ON GENETIC SEGREGATION AND THE EVOLUTION OF SEX

It has recently been argued that because the genetic load borne by an asexual species resulting from segregation, relative to a comparable sexual population, is greater than two, sex can overcome its twofold disadvantage and succeed. We evaluate some of the assumptions underlying this argument and discuss alternative assumptions. Further, we simulate the dynamics of competition between sexual and asexual types. We find that for populations of size 100 and 500 the advantages of segregation do not outweigh the cost of producing males. We conclude that, at least for small populations, drift and the cost of sex govern the evolution of sexuality, not selection or segregation. We believe, however, that if sexual and asexual populations were isolated for a sufficiently long period, segregation might impart a fitness advantage upon sexuals that could compensate for the cost of sex and allow sexuals to outcompete asexuals upon their reunion.