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.     

Spatial distribution of nests constrains the strength of sexual selection in a warbler

In socially monogamous species, extra‐pair paternity may increase the strength of intersexual selection by allowing males with preferred phenotypes to monopolize matings. Several studies have found relationships between male signals and extra‐pair mating, but many others fail to explain variation in extra‐pair mating success. A greater appreciation for the role that ecological contingencies play in structuring behavioural processes may help to reconcile contradictory results. We studied extra‐pair mating in a spatial context in the common yellowthroat (Geothlypis trichas), a territorial wood warbler. Over the course of 6 years, we observed 158 breeding attempts by 99 males, resulting in a total of 369 nests and 520 sampled nestlings. The spatial distribution of territories varied greatly, with males having between 0 and 10 close neighbours and between three and 39 neighbouring nestlings close enough to represent extra‐pair siring opportunities. Both within‐pair and extra‐pair reproductive success increased with breeding density, but the opportunity for sexual selection and strength of selection varied with density. Total variance in reproductive success was highest at low density and was mostly explained by variation in within‐pair success. In contrast, at high density, both within‐pair and extra‐pair successes contributed substantially to variance in reproductive success. The relationships between plumage and extra‐pair mating also varied by density; plumage was under strong sexual selection via extra‐pair mating success at high density, but no selection was detected at low density. Thus, ecological factors that structure social interactions can drive patterns of sexual selection by facilitating or constraining the expression of mating preferences.     

Bateman–Trivers in the 21st Century: sexual selection in a North American pitviper

Assessment of sexual selection in organisms with cryptic life histories is challenging, although accurate parentage assignments using genotypic markers, combined with behavioural observations and a method to account for open population bias, allow for robust estimation of metrics. In the present study, we employed 22 tetranucleotide microsatellite DNA loci to interpret mating and reproductive success in a population of Copperhead (Viperidae, Agkistrodon contortrix) in Connecticut, USA. We sampled DNA from 114 adults (56 males, 58 females) and 137 neonates from known mothers to quantify Bateman gradients (β_ss), as well as sex‐specific opportunities for selection (I) and sexual selection (I_s). We also estimated selection on male size [snout‐to‐vent length (SVL)], a trait important for successful combat and subsequent copulations. Estimates of male I and I_s differed significantly from those of females when estimated with four different methods and only males had a significant Bateman gradient. As predicted, male reproductive success was positively correlated with increasing SVL. These results contrast with those derived in another study investigating the same population but based solely on observational data and without correction for open population bias. We thus argue that molecular approaches to quantifying reproductive success and strength of sexual selection provide more accurate results than do behavioural observations alone. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 436–445.     

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.     

Promiscuity drives sexual selection in a socially monogamous bird

Many socially monogamous species paradoxically show signs of strong sexual selection, suggesting cryptic sources of sexual competition among males. Darwin argued that sexual selection could operate in monogamous systems if breeding sex ratios are biased or if some males attract highly fecund females. Alternatively, sexual selection might result from promiscuous copulations outside the pair bond, although several recent studies have cast doubt on this possibility, in particular by showing that variance in apparent male reproductive success (number of social young) differs little from variance in actual male reproductive success (number of young sired). Our results from a long-term study of the socially monogamous splendid fairy-wren (Malurus splendens) demonstrate that such comparisons are misleading and do not adequately assess the effects of extra-pair paternity (EPP). By partitioning the opportunity for selection and calculating Bateman gradients, we show that EPP has a strong effect on male annual and lifetime fitness, whereas other proposed mechanisms of sexual selection do not. Thus, EPP drives sexual selection in this, and possibly other, socially monogamous species.     

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.     

batemanater: a computer program to estimate and bootstrap mating system variables based on Bateman's principles

Bateman's principles continue to play a major role in the characterization of genetic mating systems in natural populations. The modern manifestations of Bateman's ideas include the opportunity for sexual selection (i.e. I_s – the variance in relative mating success), the opportunity for selection (i.e. I – the variance in relative reproductive success) and the Bateman gradient (i.e. β_ss – the slope of the least‐squares regression of reproductive success on mating success). These variables serve as the foundation for one convenient approach for the quantification of mating systems. However, their estimation presents at least two challenges, which I address here with a new Windows‐based computer software package called batemanater . The first challenge is that confidence intervals for these variables are not easy to calculate. batemanater solves this problem using a bootstrapping approach. The second, more serious, problem is that direct estimates of mating system variables from open populations will typically be biased if some potential progeny or adults are missing from the analysed sample. batemanater addresses this problem using a maximum‐likelihood approach to estimate mating system variables from incompletely sampled breeding populations. The current version of batemanater addresses the problem for systems in which progeny can be collected in groups of half‐ or full‐siblings, as would occur when eggs are laid in discrete masses or offspring occur in pregnant females. batemanater has a user‐friendly graphical interface and thus represents a new, convenient tool for the characterization and comparison of genetic mating systems.     

SEX RATIO AND DENSITY AFFECT SEXUAL SELECTION IN A SEX‐ROLE REVERSED FISH

Understanding how demographic processes influence mating systems is important to decode ecological influences on sexual selection in nature. We manipulated sex ratio and density in experimental populations of the sex‐role reversed pipefish Syngnathus typhle. We quantified sexual selection using the Bateman gradient (), the opportunity for selection (I), and sexual selection (I_s), and the maximum standardized sexual selection differential (). We also measured selection on body length using standardized selection differentials (s′) and mating differentials (m′), and tested whether the observed I and I_s differ from values obtained by simulating random mating. We found that I, I_s, and , but not , were higher for females under female than male bias and the opposite for males, but density did not affect these measures. However, higher density decreased sexual selection (m′ but not s′) on female length, but selection on body length was not affected by sex ratio. Finally, I_s but not I was higher than expected from random mating, and only for females under female bias. This study demonstrates that both sex ratio and density affect sexual selection and that disentangling interrelated demographic processes is essential to a more complete understanding of mating behavior and the evolution of mating systems.     

EXTRA‐PAIR PATERNITY AND THE VARIANCE IN MALE FITNESS IN SONG SPARROWS (MELOSPIZA MELODIA)

The variance in fitness across population members can influence major evolutionary processes. In socially monogamous but genetically polygynandrous species, extra‐pair paternity (EPP) is widely hypothesized to increase the variance in male fitness compared to that arising given the socially monogamous mating system. This hypothesis has not been definitively tested because comprehensive data describing males’ apparent (social) and realized (genetic) fitness have been lacking. We used 16 years of comprehensive social and genetic paternity data for an entire free‐living song sparrow (Melospiza melodia) population to quantify and compare variances in male apparent and realized fitness, and to quantify the contribution of the variances in within‐pair reproductive success (WPRS) and extra‐pair reproductive success (EPRS) and their covariance to the variance in realized fitness. Overall, EPP increased the variance in male fitness by only 0–27% across different fitness and variance measures. This relatively small effect reflected the presence of socially unpaired males with zero apparent and low realized fitness, small covariance between WPRS and EPRS, and large variance in WPRS that was relatively unaffected by EPP. Therefore, although EPP altered individual males’ contributions to future generations, its impact on population‐level parameters such as the opportunity for selection and effective population size was limited.     

Little effect of extrapair paternity on the opportunity for sexual selection in Savannah sparrows (Passerculus sandwichensis)

Extrapair paternity (EPP) can dramatically increase the opportunity for sexual selection if relatively few males are able to monopolize the majority of fertilizations in a population. Although recent work with birds suggests that EPP can increase the standardized variance in male reproductive success (Is) as much as 13-fold, only a male's within-pair success is typically quantified with any accuracy. In most cases, nearly half of all extrapair young are of unknown parentage. A strong, negative correlation across studies between the proportion of extrapair young for which parentage is known and the apparent effect of EPP on Is (r(s) = -0.71, P = 0.013, N = 13 studies) suggests that the incomplete sampling of extrapair sires has greatly exaggerated the influence of EPP. To achieve a more thorough accounting of EPP and its importance to variation in male fitness, we used a suite of four to six microsatellite loci to identify extrapair young and their sires in a polygynous population of Savannah sparrows (Passerculus sandwichensis). Pooling over the 2002 and 2003 breeding seasons, 79 of 116 females (68.1%) produced young outside of the pairbond and 194 of 411 offspring (47.2%) were extrapair. We identified sires for 96.4% of all young (N = 396), including sires for 92.3% of the extrapair young (N = 179), allowing us to partition Is into within-pair and extrapair components. In both years, EPP-related fitness components generated more variation in male reproductive success than the number or quality of within-pair mates. Differences among males in the number of extrapair mates alone accounted for 56.6% of Is in 2002 and for 23.6% of Is in 2003. Nonetheless, in absolute terms, the occurrence of EPP on Kent Island increased the opportunity for sexual selection less than two-fold. Averaging over the two years, Is was only 78% higher than Is,app, the variance in male reproductive success that would have occurred had EPP been nonexistent and males sired all young on their territories. Likewise, across nine socially monogamous species, we found no correlation between the extent of EPP and its effect on the opportunity for sexual selection (Is/Is,app) and only a marginally significant positive correlation between EPP and Is itself. Taken together, our results suggest that the relationship between EPP and sexual selection in birds may be much less strong and much less straightforward than commonly thought.     

Reproductive Success and Sexual Selection in Wild Eastern Tiger Salamanders (<Emphasis Type="Italic">Ambystoma t. tigrinum</Emphasis>)

Variation in reproductive success is most pronounced in species with strongly biased operational sex ratios, prominent sexual dimorphisms, and where mate competition and choice are likely. We studied sexual selection in eastern tiger salamanders (Ambystoma t. tigrinum) and examined the role of body size on reproductive success. We genotyped 155 adults and 1,341 larvae from 90 egg masses at six microsatellite loci. Parentage analyses revealed both sexes engaged in multiple matings, but was more common among females (64%) than males (27%). However, the standardized variance in mating and reproductive success was higher in males. Bateman gradients were significant and nearly identical in both sexes, suggesting that sexual selection was roughly equal between sexes. Body size was not correlated with mating or reproductive success in either sex. The apparent lack of sexual selection on body size may be a result of sperm storage, sperm competition, alternative mating tactics, and/or random induction of spermatophores.     

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.     

The mismeasurement of sexual selection

Sexual selection can explain major micro‐ and macro‐evolutionary patterns. Much of current theory predicts that the strength of sexual selection (i) is driven by the relative abundance of males and females prepared to mate (i.e. the operational sex ratio, OSR) and (ii) can be generally estimated by calculating intra‐sexual variation in mating success (e.g. the opportunity for sexual selection, I_s). Here, we demonstrate the problematic nature of these predictions. The OSR and I_s only accurately predict sexual selection under a limited set of circumstances, and more specifically, only when mate monopolization is extremely strong. If mate monopolization is not strong, using OSR or I_s as proxies or measures of sexual selection is expected to produce spurious results that lead to the false conclusion that sexual selection is strong when it is actually weak. These findings call into question the validity of empirical conclusions based on these measures of sexual selection.     

Mating systems and predictors of relative reproductive success in a Cutthroat Trout subspecies of conservation concern

Mating systems and patterns of reproductive success in fishes play an important role in ecology and evolution. While information on the reproductive ecology of many anadromous salmonids (Oncorhynchus spp.) is well detailed, there is less information for nonanadromous species including the Yellowstone Cutthroat Trout (O. clarkii bouvieri), a subspecies of recreational angling importance and conservation concern. Using data from a parentage‐based tagging study, we described the genetic mating system of a migratory population of Yellowstone Cutthroat Trout, tested for evidence of sexual selection, and identified predictors of mating and reproductive success. The standardized variance in mating success (i.e., opportunity for sexual selection) was significantly greater for males relative to females, and while the relationship between mating success and reproductive success (i.e., Bateman gradient) was significantly positive for both sexes, a greater proportion of reproductive success was explained by mating success for males (r ² = 0.80) than females (r ² = 0.59). Overall, the population displayed a polygynandrous mating system, whereby both sexes experienced variation in mating success due to multiple mating, and sexual selection was variable across sexes. Tests for evidence of sexual selection indicated the interaction between mating success and total length best‐predicted relative reproductive success. We failed to detect a signal of inbreeding avoidance among breeding adults, but the group of parents that produced progeny were on average slightly less related than adults that did not produce progeny. Lastly, we estimated the effective number of breeders (N _b) and effective population size (N _e) and identified while N _b was lower than N _e, both are sufficiently high to suggest Yellowstone Cutthroat Trout in Burns Creek represent a genetically stable and diverse population.     

Experimental evidence that brighter males sire more extra‐pair young in tree swallows

Across taxa, extra‐pair mating is widespread among socially monogamous species, but few studies have identified male ornamental traits associated with extra‐pair mating success, and even fewer studies have experimentally manipulated male traits to determine whether they are related directly to paternity. As a consequence, there is little experimental evidence to support the widespread hypothesis that females choose more ornamented males as extra‐pair mates. Here, we conducted an experimental study of the relationship between male plumage colour and fertilization success in tree swallows (Tachycineta bicolor), which have one of the highest levels of extra‐pair mating in birds. In this study, we experimentally dulled the bright blue plumage on the back of males (with nontoxic ink markers) early in the breeding season prior to most mating. Compared with control males, dulled males sired fewer extra‐pair young, and, as a result, fewer young overall. Among untreated males, brighter blue males also sired more extra‐pair young, and in paired comparisons, extra‐pair sires had brighter blue plumage than the within‐pair male they cuckolded. These results, together with previous work on tree swallows, suggest that extra‐pair mating behaviour is driven by benefits to both males and females.     

Comprehensive paternity assignment: genotype,spatial location and social status in song sparrows,Melospiza Melodia

Comprehensive, accurate paternity assignment is critical to answering numerous questions in evolutionary ecology. Yet, most studies of species with extra‐pair paternity (EPP) fail to assign sires to all offspring. Common limitations include incomplete and biased sampling of offspring and males, particularly with respect to male location and social status, potentially biasing estimated patterns of paternity. Studies that achieve comprehensive sampling and paternity assignment are therefore required. Accordingly, we genotyped virtually all males and >99% of 6‐day‐old offspring over 16 years in a song sparrow (Melospiza melodia) population and used three complementary statistical methodologies to attempt complete paternity assignment for all 2207 offspring. Assignments were highly consistent across maximum likelihood methods that used solely genotype data, and heuristic and integrated Bayesian analyses that included data describing individual locations. Sires were assigned to >99% of all genotyped offspring with ≥95% confidence, revealing an EPP rate of c. 28%. Extra‐pair sires primarily occupied territories neighbouring their extra‐pair offspring; spatial location was therefore highly informative for paternity assignment. EPP was biased towards paired territorial males, although unpaired territorial and floater males sired c. 13% of extra‐pair offspring. Failing to sample and include unpaired males as candidate sires would therefore substantially reduce assignment rates. These analyses demonstrate the integration of genetic and ecological information to achieve comprehensive paternity assignment and direct biological insight, illustrate the potential biases that common forms of incomplete sampling could have on estimated patterns of EPP, and provide an essential basis for understanding the evolutionary causes and consequences of EPP.     

An integrative mating system assessment of a nonmodel,economically important Pacific rockfish (Sebastes melanops) reveals nonterritorial polygamy and conservation implications for a large species flock

Characterizing the mating systems of long‐lived, economically important Pacific rockfishes comprising the viviparous Sebastes species flock is crucial for their conservation. However, direct assignment of mating success to sires is precluded by open, offshore populations and high female fecundity. We addressed this challenge by integrating paternity‐assigned mating success of females with the adult sex ratio (ASR) of the population, male evolutionary responses to receptive females, and reproductive life history traits—in the framework of sexual selection theory—to assess the mating system of Sebastes melanops. Microsatellite parentage analysis of 17 pregnant females, 1,256 of their progeny, and 106 adults from the population yielded one to four sires per brood, a mean of two sires, and a female mate frequency distribution with a truncated normal (random) pattern. The 11 multiple paternity broods all contained higher median allele richness than the six single paternity broods (Wilcoxon test: W = 0, p < .001), despite similar levels of average heterozygosity. By sampling sperm and alleles from different males, polyandrous females gain opportunities to enhance their sperm supply and to lower the cost of mating with genetically incompatible males through reproductive compensation. A mean of two mates per mated female with a variance of one, an ASR = 1.2 females per male, and the expected population mean of 2.4 mates for mated males (and the estimated 35 unavailable sires), fits polygamous male mate frequency distributions that distinguish polygynandry and polyandrogyny mating systems, that is, variations of polygamy, but not polyandry. Inference for polygamy is consistent with weak premating sexual selection on males, expected in mid‐water, schooling S. melanops, owing to polyandrous mating, moderately aggregated receptive females, an even ASR, and no territories and nests used for reproduction. Each of these characteristics facilitates more mating males and erodes conspicuous sexual dimorphism. Evaluation of male evolutionary responses of demersal congeners that express reproductively territorial behavior revealed they have more potential mechanisms for producing premating sexual selection, greater variation in reproductive success, and a reduced breeding effective population size of adults and annual effective size of a cohort, compared to S. melanops modeled with two mates per adult. Such divergence in behavior and mating system by territorial species may differentially lower their per capita birth rates, subsequent population growth, and slow their recovery from exploitation.     

Multiple paternity is a shared reproductive strategy in the live‐bearing surfperches (Embiotocidae) that may be associated with female fitness

According to Bateman's principle, female fecundity is limited relative to males, setting the expectation that males should be promiscuous, while females should be choosy and select fewer mates. However, several surfperches (Embiotocidae) exhibit multiple paternity within broods indicating that females mate with multiple males throughout the mating season. Previous studies found no correlation between mating success and reproductive success (i.e., a Bateman gradient). However, by including samples from a broader range of reproductive size classes, we found evidence of a Bateman gradient in two surfperch species from distinct embiotocid clades. Using microsatellite analyses, we found that 100% of the spotfin surfperch families sampled exhibit multiple paternity (Hyperprosopon anale, the basal taxon from the only clade that has not previously been investigated) indicating that this tactic is a shared reproductive strategy among surfperches. Further, we detected evidence for a Bateman gradient in H. anale; however, this result was not significant after correction for biases. Similarly, we found evidence for multiple paternity in 83% of the shiner surfperch families (Cymatogaster aggregata) sampled. When we combine these data with a previous study on the same species, representing a larger range of reproductive size classes and associated brood sizes, we detect a Bateman gradient in shiner surfperch for the first time that remains significant after several conservative tests for bias correction. These results indicate that sexual selection is likely complex in this system, with the potential for conflicting optima between sexes, and imply a positive shift in fertility (i.e., increasing number) and reproductive tactic with respect to the mating system and number of sires throughout the reproductive life history of females. We argue that the complex reproductive natural history of surfperches is characterized by several traits that may be associated with cryptic female choice, including protracted oogenesis, uterine sac complexity, and sperm storage.     

Fitness benefits of polyandry for experienced females

Females often mate with several different males, which may promote sperm competition and increase offspring viability. However, the potential benefits of polyandry remain controversial, particularly in birds where recent reviews have suggested that females gain few genetic benefits from extra‐pair mating. In tree swallows (Tachycineta bicolor), we found that females with prior breeding experience had more sires per brood when paired to genetically similar social mates, and, among experienced females, broods with more sires had higher hatching success. Individual females breeding in two consecutive years also produced broods with more sires when they were more genetically similar to their mate. Thus, experienced females were able to avoid the costs of mating with a genetically similar social mate and realize fitness benefits from mating with a relatively large number of males. This is one of the first studies to show that female breeding experience influences polyandry and female fitness in a natural population of vertebrates. Our results suggest that the benefits of polyandry may only be clear when considering both the number of mates females acquire and their ability to modify the outcome of sexual conflict.     

Individual Quality and Extra-Pair Paternity in the Blue Tit: Sexy Males Bear the Costs

Adaptive explanations for the evolution of extra-pair paternity (EPP) suggest that females seek extra-pair copulations with high quality males. Still, the link between ornamentation, individual quality, and paternity remains unclear. Moreover, honest signaling is essential when explaining EPP because it is needed for sexual selection to occur; yet, it is understudied in multiple ornaments. Because blue tits (Cyanistes caeruleus) show variable color expression in several plumage patches, we tested: (i) over two seasons, whether males in better condition, more ornamented and less infected by blood parasites gain EPP and have higher reproductive success, and (ii) over three seasons, whether mating patterns affect color change. Males with more saturated yellow feathers, brighter tails, and in better condition had higher reproductive success in one of the seasons. Contrary to expectation, in another season, males that gained EPP were parasitized by blood parasites, suggesting increased vector exposure during extra-pair copulations. Our results for two seasons show that males siring more extra-pair young were older and grew brighter cheek or tail feathers for the following season. Despite the increased mating costs, in socially monogamous avian systems, high quality males incur in EPP without compromising traits that may be under sexual selection.