Plumage polymorphism and fitness in Swainson’s hawks

We examine the maintenance of a plumage polymorphism, variation in plumages among the same age and sex class within a population, in a population of Swainson’s Hawks. We take advantage of 32 years of data to examine two prevalent hypotheses used to explain the persistence of morphs: apostatic selection and heterozygous advantage. We investigate differences in fitness among three morph classes of a melanistic trait in Swainson’s Hawks: light (7% of the local breeding population), intermediate (57%) and dark (36%). Specifically, we examined morph differences in adult apparent survival, breeding success, annual number of fledglings produced, probability of offspring recruitment into the breeding population and lifetime reproductive success (LRS). If apostatic selection were a factor in maintaining morphs, we would expect that individuals with the least frequent morph would perform best in one or more of these fitness categories. Alternatively, if heterozygous advantage played a role in the maintenance of this polymorphism, we would expect heterozygotes (i.e. intermediate morphs) to have one or more increased rates in these categories. We found no difference in adult apparent survival between morph classes. Similarly, there were no differences in breeding success, nest productivity, LRS or probability of recruitment of offspring between parental morph. We conclude that neither apostatic selection nor heterozygous advantage appear to play a role in maintaining morphs in this population.     

Morph‐dependent fitness and directional change of morph frequencies over time in a Dutch population of Common buzzards Buteo buteo

How genetic polymorphisms are maintained in a population is a key question in evolutionary ecology. Previous work on a plumage colour polymorphism in the common buzzard Buteo buteo suggested heterozygote advantage as the mechanism maintaining the co‐existence of three morphs (light, intermediate and dark). We took advantage of 20 years of life‐history data collected in a Dutch population to replicate earlier studies on the relationship between colour morph and fitness in this species. We examined differences between morphs in adult apparent survival, breeding success, annual number of fledglings produced and cumulative reproductive success. We found that cumulative reproductive success differed among morphs, with the intermediate morph having highest fitness. We also found assortative mating for colour morph, whereby assortative pairs were more likely to produce offspring and had longer‐lasting pair bonds than disassortative pairs. Over the 20‐year study period, the proportion of individuals with an intermediate morph increased. This apparent evolutionary change did not just arise from selection on individual phenotypes, but also from fitness benefits of assortative mating. The increased frequency of intermediates might also be due to immigration or drift. We hypothesize that genetic variation is maintained through spatial variation in selection pressures. Further studies should investigate morph‐dependent dispersal behaviour and habitat choice.     

Aggression and fitness differences between plumage morphs in the common buzzard (Buteo buteo)

Genetic plumage polymorphism in birds is increasingly recognizedas a potentially important trait influencing birds’ lifehistories. In the common buzzard Buteo buteo, the 3 color morphsvary in lifetime reproductive success (LRS), but the proximatemechanisms leading to these differences are unknown. We firstconfirmed the stability of the fitness differences found previously,using a greatly extended LRS data set. To find potential causesfor these differences, we experimentally studied variation inaggressive behavior of the morphs, both against an interspecificpredator and intraspecific competitors. The morphs showed substantialvariation in aggressive behavior. Light-colored males were mostaggressive toward an interspecific predator, followed by intermediateand dark males. In females, this pattern was reversed, resultingin sex-related differences of aggression in 2 morphs. When defendingtheir territory against intraspecific competitors, no absolutedifference in aggression was found, but the morphs reacted strongesttoward intruders of a morph similar to their own. This suggeststhat aggression differs both between and within morphs, leadingto a complex pattern on the population level. Coupled with thestrong fitness differences, our results suggest that the geneticbasis of the polymorphism has far-reaching behavioral consequences.     

Variation at phenological candidate genes correlates with timing of dispersal and plumage morph in a sedentary bird of prey

Polymorphic genes involved in the conserved molecular signalling of circadian and circannual clocks may play important roles in governing the timing of breeding and dispersal and thereby affect fitness in vertebrates. However, relatively few studies have explored associations between phenological candidate genes and behaviour, and these are somewhat biased towards particular taxonomic groups such as passerine birds and salmonid fish. Consequently, we assayed microsatellite polymorphisms within the exonic and 3′ untranslated regions of the regulatory genes CLOCK, NPAS2, ADCYAP1 and CREB1 in the common buzzard (Buteo buteo), a polymorphic raptor species with three plumage morphs that differ in key life history traits including lifetime reproductive success. In contrast to studies of passerines, CLOCK poly‐glutamine (poly‐Q) was found to be monomorphic in 976 common buzzard nestlings as well as in three other Buteo species. Moreover, none of the candidate genes were significantly associated with fledging dates, although intermediately melanized females were found to lay earlier on average than light or dark morph individuals, and their offspring carried longer ADCYAP1 alleles. In contrast, all three candidate genes explained significant variation in one or more measures of juvenile buzzard dispersal (resighting probability, timing of dispersal and distance dispersed). Our findings contribute towards a broader body of work on the adaptive significance of CLOCK polymorphism, while also building upon previous studies that have documented links between ADCYAP1 variability and the timing of migration.     

Lifetime offspring production in relation to breeding lifespan, attractiveness, and mating status in male collared flycatchers

As a comprehensive fitness parameter, lifetime reproductive success (LRS) is influenced by many different environmental and genetic factors, among which longevity is one of the most important. These factors can be reflected in secondary sexual characters, which may affect the life histories of individuals via social relations with conspecifics. Facultative polygyny in birds is another conspicuous reproductive trait that potentially increases male reproductive success, but lifetime success data in relation to polygyny are scarce. Here, we used 17?years of breeding data to quantify the LRS of male collared flycatchers (Ficedula albicollis) on the basis of lifetime recruitment of offspring. Breeding lifespan showed a positive relationship with LRS, and it was also significantly associated with mean recruitment of offspring per breeding year. Body size and sexually selected forehead patch size did not predict the number of recruits. Polygyny was positively associated with LRS, but when we corrected for lifespan, this relationship disappeared. Our results demonstrate that the relationship between longevity and LRS is not explained by the higher number of reproductive attempts when living longer, and question the adaptive value of polygyny in this population. The lack of association between forehead patch size and recruitment suggests that forehead patch is a poor indicator of phenotypic quality in our birds.     

The adaptive significance of colour pattern polymorphism in the Australian scincid lizard Lampropholis delicata

Females of Lampropholis delicata are dimorphic for colour pattern, the difference between morphs being the presence or absence of a distinct white mid-lateral stripe. A less distinct striped morph occurs also in males. We evaluated alternative hypotheses for the maintenance of this polymorphism by examining temporal and spatial variation in morph frequency, testing for differential selection among morphs using data on body size and reproductive traits from preserved specimens, and experimentally manipulating colour pattern in free-ranging lizards of both sexes, to assess the influence of the lateral stripe on survival rates. We found that the relative frequency of striped individuals varied among populations and decreased from north to south in both sexes, coincident with an increasing incidence of regenerated tails. Morph frequencies did not change through time within a population. Striped gravid females appeared to survive better and produced larger clutches than did non-striped females. In our experimental study, the relationship between survival and colour morph differed between the two sexes; males painted with a white lateral stripe had lower survival than control (brown stripe) males, but survival did not differ between striped and control females. The different response in the two sexes may be due partly to differences in temperature and microhabitat selection. We propose that the white lateral stripe decreases susceptibility to predators in gravid females but increases risk of predation in males, especially in combination with low temperatures. The polymorphism might be maintained by: (1) opposing fitness consequences of the stripe in males and females; (2) sex-specific habitat selection; and (3) gene flow in combination with spatial variation in relative fitness of the two morphs.     

Seasonal trade-offs in cell-mediated immunosenescence in ruffs (Philomachus pugnax)

The immune system is an energetically expensive self-maintenance complex that, given the risks of parasitism, cannot be carelessly compromised. Life-history theory posits that trade-offs between fitness components, such as self-maintenance and reproduction, vary between genders and age classes depending on their expected residual lifetime reproductive success, and seasonally as energetic requirements change. Using ruff (Philomachus pugnax), a bird with two genetically distinct male morphs, we demonstrate here a decrease in male immunocompetence during the breeding season, greater variance in immune response among males than females, immunosenescence in both sexes and male morphs, and a seasonal shift in the age range required to detect senescence. Using a phytohaemagglutinin delayed hypersensitivity assay, we assessed cell-mediated immunity (CMI) of males of typical breeding age during the breeding and nonbreeding seasons, and of a larger sample that included females and birds of a greater age range during the non-breeding period. CMI was higher for breeding-aged males in May than in November, but the increase was not related to age or male morph. In November, mean CMI did not differ between the sexes, but the variance was higher for males than for females, and there were no differences in mean or variance between the two male morphs. For both sexes and male morphs, CMI was lower for young birds than for birds of typical breeding ages, and it declined again for older birds. In males, senescence was detected in the non-breeding season only when very old birds were included. These results, generally consistent with expectations from life-history theory, indicate that the immune system can be involved in multifarious trade-offs within a yearly cycle and along an individual's lifetime, and that specific predictions about means and variances in immune response should be considered in future immunoecological research.     

Sex differences in relationships between habitat use and reproductive performance in Soay sheep (Ovis aries)

The role of habitat use in generating individual variation in fitness has rarely been examined empirically in natural populations of long‐lived mammals, particularly for both sexes simultaneously. This is the case despite the increase in studies attempting to understand evolutionary change in such populations. Using data from the St. Kilda Soay sheep population, we quantified the association between lifetime reproductive performance (lifetime breeding and reproductive success) and the proportion of the home range covered by a key grass species, H. lanatus, for 490 females and 304 males. Increased H. lanatus cover was associated only with increased female lifetime reproductive success, but increased lifetime breeding success for both sexes, arising through increased male longevity and increased female fecundity. This work suggests that improved understanding of the causes and consequences of fitness differences will likely require us to better account for habitat‐derived individual variation, and to do so for the sexes appropriately.     

Territory Quality and Plumage Morph Predict Offspring Sex Ratio Variation in a Raptor

Parents may adapt their offspring sex ratio in response to their own phenotype and environmental conditions. The most significant causes for adaptive sex-ratio variation might express themselves as different distributions of fitness components between sexes along a given variable. Several causes for differential sex allocation in raptors with reversed sexual size dimorphism have been suggested. We search for correlates of fledgling sex in an extensive dataset on common buzzards Buteo buteo, a long-lived bird of prey. Larger female offspring could be more resource-demanding and starvation-prone and thus the costly sex. Prominent factors such as brood size and laying date did not predict nestling sex. Nonetheless, lifetime sex ratio (LSR, potentially indicative of individual sex allocation constraints) and overall nestling sex were explained by territory quality with more females being produced in better territories. Additionally, parental plumage morphs and the interaction of morph and prey abundance tended to explain LSR and nestling sex, indicating local adaptation of sex allocation However, in a limited census of nestling mortality, not females but males tended to die more frequently in prey-rich years. Also, although females could have potentially longer reproductive careers, a subset of our data encompassing full individual life histories showed that longevity and lifetime reproductive success were similarly distributed between the sexes. Thus, a basis for adaptive sex allocation in this population remains elusive. Overall, in common buzzards most major determinants of reproductive success appeared to have no effect on sex ratio but sex allocation may be adapted to local conditions in morph-specific patterns.     

Correlates of lifetime reproductive success in three species of European ducks

Number of breeding attempts is a strong correlate of lifetime reproductive success (LRS) in birds, but the relative importance of potentially interacting factors affecting LRS has rarely been fully evaluated. We considered simultaneously five main factors hypothesized to influence LRS (age at first breeding, nesting date, number of breeding attempts, female traits, brood parasitism) by analyzing with path analysis 22-year data sets for 1,279 individually marked females and their offspring in tufted duck (Aythya fuligula), common pochard (A. ferina) and northern shoveler (Anas clypeata). We recaptured marked offspring as breeding adults (n=496 females) and obtained more complete estimates of LRS by incorporating information about banded ducklings of both sexes shot by hunters 12 months after banding (n=138). In tufted ducks and especially pochard (both diving duck species), late-hatched females tended to delay nesting until 2-years old. Most females (tufted duck, 74%; pochard, 71%; shoveler, 59%) apparently produced no breeding-age offspring. Number of breeding attempts (i.e., longevity) was the strongest correlate of LRS in all species, after controlling effects of age at first breeding, relative nest initiation date, wing length and body mass. Percentage of females producing recruits increased gradually with number of breeding attempts for all three species. Also, as expected, females nesting early in the breeding season had higher LRS than late-nesting individuals. In shoveler, female-specific characteristics of relatively longer wings and heavier late incubation body mass had positive effects on LRS, the latter feature being more common in 2-year-old nesters. In diving ducks, no relationships were detected between LRS and female-specific traits like wing length or body mass, and nor did acceptance of parasitic eggs have any deleterious impact on fitness estimates. Overall, number of fledged ducklings and LRS were related in tufted duck, weakly associated in pochard and unrelated in shoveler, implying that fledging success is not always a reliable measure of LRS.     

Telomere length in relation to colour polymorphism across life stages in the tawny owl

Telomere erosion has been proposed to be tightly associated with senescence, environmental stressors and life history trade‐offs. How telomere dynamics vary across life stages and especially in relation to (heritable) phenotypic traits is still unclear. The tawny owl Strix aluco display a highly heritable melanin‐based colour polymorphism, a grey and a brown morph, linked to several fitness traits including morph‐specific telomere dynamics. As adults, brown tawny owls have shorter relative telomere length (RTL) and exhibit faster telomere shortening rate than grey owls. Here we test if these morph‐specific telomere dynamics emerge already during growth, or if they are induced only in adult life through differential physiological costs associated with the life history of the morphs. We analysed RTL from 287 tawny owl offspring and 81 first breeding adults to evaluate at what life stage morph‐specific patterns emerge. We found no differences in RTL between the two morphs during the nestling period nor at the first breeding attempt. Sex, brood size or size rank in the nest did not affect offspring RTL. Among first‐breeders, females had shorter telomeres than males suggesting a sampling‐time dependent difference in reproductive costs between sexes, due to the prominent sex roles in tawny owls in the early nestling period. The probability to return to breed after the first breeding attempt was not affected by RTL, sex or colour morph. The lack of morph‐specific difference in RTL among nestlings and first breeders suggests that previously observed morph‐specific differences in RTL dynamics in adults emerge at the onset of the breeding career and is likely due to different physiological profiles and life‐history strategies adopted by adults. We conclude that different telomere dynamics and senescence patterns among highly heritable phenotypes (colour morphs) are likely to be a result of differential costs of reproduction and self‐maintenance.     

Maladaptive mate choice maintained by heterozygote advantage

Common buzzards (Buteo buteo) show a plumage polymorphism that appears to be maintained by heterozygote advantage and allows a maladaptive form of mate choice to persist. The light and dark morphs have a much lower fitness than the presumed heterozygous intermediate morph, but are replenished through Mendelian segregation in intermediate-intermediate pairs. Light and dark morphs could maximize their fitness by mating light with dark to produce all intermediate offspring, but instead choose partners of their own color, thereby producing broods of minimally fit homozygotes. Such maladaptive behavior argues forcefully against mate choice based on "good genes," and its persistence is best explained by heterozygote advantage maintaining the polymorphism coupled with nongenetic mate choice based on sexual imprinting. Modeling different patterns of mate choice shows that random mating and preference for own morph fit our data poorly, whereas preference for mother's morph yields a good fit.     

Endocrine correlates of alternative phenotypes in the white-throated sparrow (Zonotrichia albicollis)

Many vertebrate species exhibit alternative phenotypes (or morphs), in which one sex displays phenotypic variation equal to or greater than the variation between the sexes. Males in such species typically display differences in reproductive strategies and morphology. Steroid hormones such as testosterone are known modulators of reproductive behavior and morphology and therefore are obvious candidates for the mediation of phenotypic differences between morphs. We conducted a year-round study in the white-throated sparrow (Zonotrichia albicollis) that exhibits alternative phenotypes in plumage coloration and behavior in both sexes: during the breeding season, white-striped males and females are more aggressive and have higher song rates than tan-striped individuals. At the beginning of the breeding season, free-living white-striped males had higher plasma testosterone concentrations than tan-striped males. However, this finding might have been due to different social experiences because captive male morphs sampled at similar times of year did not differ in testosterone concentrations. Captive white-striped males had larger testis and cloacal protuberance sizes than tan-striped males, which might be related to the divergent mating strategies of the morphs. Male morphs showed similar increases in luteinizing hormone following injections of gonadotropin-releasing hormone, but white-striped males showed larger increases in testosterone, indicating differences between morphs in gonadal testosterone production. Females had low concentrations of testosterone, and morphs did not differ. Plasma dehydroepiandrosterone (DHEA) concentrations were elevated in both sexes and morphs during the breeding and non-breeding seasons. These data do not support the hypothesis that testosterone activates behavioral differences between alternative phenotypes in the white-throated sparrow. Alternative testable hypotheses include hormonal effects during early development and direct genetic effects.     

Male brood provisioning rates provide evidence for inter‐age competition for mates in female Cooper's Hawks Accipiter cooperii

Life history theory predicts that individuals should maximize lifetime reproductive success (LRS) by breeding as soon as they reach sexual maturity, yet many species delay breeding, either because there are insufficient available mates or breeding sites, or because delayed breeding yields higher LRS. Accipitriform species, such as Cooper's Hawk Accipiter cooperii, exhibit both delayed breeding and delayed plumage maturation. However, in certain circumstances, first‐year females in non‐definitive plumage do breed and apparently compete with older females for high‐quality breeding territories. We predicted that these young females are at a competitive disadvantage compared with older females and that older females would have both higher reproductive success and be able to acquire higher quality nesting territories. We conducted brood counts and measured prey delivery rates by male Cooper's Hawks in an expanding urban population located in Albuquerque, New Mexico (USA), to assess our prediction. We found that older females had higher reproductive success, fledging 1.6 more offspring than younger females, and that they occupied territories where males provisioned at higher rates of 0.37 more prey items per 2‐h period. Our results showed that older females fared better than first‐year females but it is unclear if this is the result of passive or active competition. Older females initiated nesting 14.3 days sooner than first‐year females and thus may have filled vacant, high‐quality territories before first‐year females began seeking mates. Additionally, first‐year females were never observed persistently to confront older females for breeding territories, but they did actively compete against each other. First‐year females may defer to older females who, in a direct competitive interaction, would be most likely to prevail. Thus, delayed plumage maturation in Cooper's Hawks may serve to focus competition for nesting territories within age classes.     

Colour Polymorphism and Alternative Breeding Strategies: Effects of Parent’s Colour Morph on Fitness Traits in the Common Wall Lizard

Colour polymorphism (CP) is widespread in animals, but mechanisms underlying morph evolution and maintenance are not completely resolved. In reptiles, CP is often genetically based and associated with alternative behavioural strategies, mainly in males for most cases. However, female colour morphs also display alternative reproductive strategies associated with behavioural and physiological traits, which may contribute to maintain CP in the population. Both sexes of the common wall lizard (Podarcis muralis) show three pure colour morphs, white, yellow and red. Here, we looked for the effects of male and female colour morphs on fitness traits of captive-breeding pairs. All yellow-throated females laid clutches of many small eggs and produced many light offspring, behaving as r-strategists, whereas white-throated females laid clutches of few large eggs and produced few heavy offspring, behaving as K-strategists. Red-throated females adopted a conditional Kr-strategy depending on their size/age. These basic female strategies were modulated in relation to mate morph: white females had the best fitness gain in terms of viable offspring when mated to red males; mating between yellow morphs yielded a greater breeding success than all other morph crosses, but also lighter offspring; finally, red females produced heavy progeny when paired with red or white males, and light offspring in pair with yellow males. Thus, correlation between CP and traits relevant to fitness combined with non-random mating, either assortative or disassortative, could increase the potential for CP to contribute to divergent evolution in the common wall lizard.     

Live fast, die young: trade-offs between fitness components and sexually antagonistic selection on weaponry in Soay sheep

Males are predicted to compete for reproductive opportunities, with sexual selection driving the evolution of large body size and weaponry through the advantage they confer for access to females. Few studies have explored potential trade-offs of investment in secondary sexual traits between different components of fitness or tested for sexually antagonistic selection pressures. These factors may provide explanations for observed polymorphisms in both form and quality of secondary sexual traits. We report here an analysis of selection on horn phenotype in a feral population of Soay sheep (Ovis aries) on the island of Hirta, St. Kilda, Scotland. Soay sheep display a phenotypic polymorphism for horn type with males growing either normal or reduced (scurred) horns, and females growing either normal, scurred, or no (polled) horns; further variation in size exists within horn morphs. We show that horn phenotype and the size of the trait displayed is subject to different selection pressures in males and females, generating sexually antagonistic selection. Furthermore, there was evidence of a trade-off between breeding success and longevity in normal-horned males, with both the normal horn type and larger horn size being associated with greater annual breeding success but reduced longevity. Therefore, selection through lifetime breeding success was not found to act upon horn phenotype in males. In females, a negative association of annual breeding success within the normal-horned phenotype did not result in a significant difference in lifetime fitness when compared to scurred individuals, as no significant difference in longevity was found. However, increased horn size within this group was negatively associated with breeding success and longevity. Females without horns (polled) suffered reduced longevity and thus reduced lifetime breeding success relative the other horn morphs. Our results therefore suggest that trade-offs between different components of fitness and antagonistic selection between the sexes may maintain genetic variation for secondary sexual traits within a population.     

Multiple signaling functions of song in a polymorphic species with alternative reproductive strategies

Vocal traits can be sexually selected to reflect male quality, but may also evolve to serve additional signaling functions. We used a long‐term dataset to examine the signaling potential of song in dimorphic white‐throated sparrows (Zonotrichia albicollis). We investigated whether song conveys multifaceted information about the vocalizing individual, including fitness, species identity, individual identity, and morph. We also evaluated whether song traits correlate differently with fitness in the two morphs, as the more promiscuous strategy of white, relative to tan, morph males might impose stronger sexual selection. Males with high song rates achieved higher lifetime reproductive success, and this pattern was driven by white morph males. In addition, males that sang songs with many notes survived longer, but this pattern was less robust. Thus, song traits reflect differences in fitness and may more strongly affect fitness in the white morph. Song frequency was unrelated to fitness, body size, or morph, but was individual specific and could signal individual identity. Songs of the two morphs displayed similar frequency ratios and bandwidths. However, tan morph males sang songs with longer first notes, fewer notes, and higher variability. Thus, song could be used in morph discrimination. Variation in frequency ratios between notes was low and could function in conspecific recognition, but pitch change dynamics did differ between four different song types observed. Our results support a multiple messages model for white‐throated sparrow song, in which different song traits communicate discrete information about the vocalizing individual.     

No correlation between multi‐locus heterozygosity and fitness in the common buzzard despite heterozygote advantage for plumage colour

Correlations between heterozygosity and fitness are frequently found but rarely well understood. Fitness can be affected by single loci of large effect which correlate with neutral markers via linkage disequilibrium, or as a result of variation in genome‐wide heterozygosity following inbreeding. We explored these alternatives in the common buzzard, a raptor species in which three colour morphs differ in their lifetime reproductive success. Using 18 polymorphic microsatellite loci, we evaluated potential genetic differences among the morphs which may lead to subpopulation structuring and tested for correlations between three fitness‐related traits and heterozygosity, both genome wide and at each locus separately. Despite their assortative mating pattern, the buzzard morphs were found to be genetically undifferentiated. Multilocus heterozygosity was only found to be correlated with a single fitness‐related trait, infection with the blood parasite, Leucocytozoon buteonis, and this was via interactions with vole abundance and age. One locus also showed a significant relationship with blood parasite infection and ectoparasite infestation. The vicinity of this locus contains two genes, one of which is potentially implicated in the immune system of birds. We conclude that genome‐wide heterozygosity is unlikely to be a major determinant of parasite burden and body condition in the polymorphic common buzzard.     

Delayed breeding affects lifetime reproductive success differently in male and female green woodhoopoes

In cooperatively breeding species, many individuals only start breeding long after reaching physiological maturity [1], and this delay is expected to reduce lifetime reproductive success (LRS) [1-3]. Although many studies have investigated how nonbreeding helpers might mitigate the assumed cost of delayed breeding (reviewed in [3]), few have directly quantified the cost itself [4, 5] (but see [6, 7]). Moreover, although life-history tradeoffs frequently influence the sexes in profoundly different ways [8, 9], it has been generally assumed that males and females are similarly affected by a delayed start to breeding [7]. Here, we use 24 years of data to investigate the sex-specific cost of delayed breeding in the cooperatively breeding green woodhoopoe (Phoeniculus purpureus) and show that age at first breeding is related to LRS differently in males and females. As is traditionally expected, males that started to breed earlier in life had greater LRS than those that started later. However, females showed the opposite pattern: Those individuals that started to breed later in life actually had greater LRS than those that started earlier. In both sexes, the association between age at first breeding and LRS was driven by differences in breeding-career length, rather than per-season productivity. We hypothesize that the high mortality rate of young female breeders, and thus their short breeding careers, is related to a reduced ability to deal with the high physiological costs of reproduction in this species. These results demonstrate the importance of considering sex-specific reproductive costs when estimating the payoffs of life-history decisions and bring into question the long-held assumption that delayed breeding is necessarily costly.