Pigment allocation to eggs decreases plasma antioxidants in a songbird

Although evidence is accumulating on the adaptive function of female ornamentation, very little is known about maternal allocation decisions involving sexual signaling and other reproductive functions. Blue egg coloration has been suggested as a sexually selected signal of female quality to males, and some recent studies are in accordance with this hypothesis. Blue eggshell coloration results from the deposition of biliverdin pigment by laying females, which is a potent antioxidant. Thus, egg pigmentation should be costly in terms of antioxidants, an assumption of the signaling hypothesis that has not been tested yet. We induced increased reproductive effort in a set of female pied flycatchers Ficedula hypoleuca through nest removal and measured egg pigmentation and plasma antioxidant levels in relation with a control group. Experimental females showed a negative association between egg color and plasma antioxidant levels, while there was no relationship for control birds. This supports that egg pigmentation is costly in terms of general antioxidant defenses and suggests a tradeoff between the allocations to both traits. Furthermore, experimental females with more colorful eggs raised more fledglings, especially when breeding early. Controls did not show a relationship between egg color and reproductive success. Females laying more colorful eggs could have shifted their allocation decisions towards current reproduction, at the expense of their own antioxidant defenses. Our results highlight that blue egg coloration is a life-history trait, subject to tradeoffs with other attributes, and seems to be especially informative under harsh breeding conditions.     

Egg pigmentation reflects female and egg quality in the spotless starling <Emphasis Type="Italic">Sturnus unicolor</Emphasis>

It has been proposed that blue colouration in eggs has evolved as a signal of female quality that males can use to modulate their parental investment. This hypothesis is based in the antioxidant properties of biliverdin whose costly deposition in the eggshell is expected to signal female antioxidant capacity and egg quality. Since maternally derived androgens are costly to produce and may adaptively affect offspring phenotype, high-quality females may benefit by signalling their androgen investment through egg colouration. Our aim was to investigate whether egg colour variation in the spotless starling reflected the amount of pigments on the eggshell and whether egg pigmentation was related to female and egg quality. Chromatography analyses revealed that spotless starling eggshells contained two different pigments: biliverdin and protoporphyrin IX with no correlation between them. Biliverdin contents correlated positively with egg colouration indicating that darker eggs with a higher peak in the blue–green segment of the spectrum contained higher amounts of biliverdin. Eggs containing more biliverdin were laid by high-quality females and contained higher yolk testosterone levels. However, despite the strong correlation between biliverdin and colorimetric variables, egg colouration did not reflect accurately female and egg quality. Our results provide evidence that eggshell pigmentation in the spotless starling is related to female and egg quality as shown by the yolk testosterone levels. However, the lack of relation between egg colour and female condition and egg quality do not provide evidence to support the signalling function of egg colouration.     

Egg coloration is correlated with female condition in eastern bluebirds (Sialia sialis)

Egg coloration has been hypothesized to reflect female condition. Because of the proposed physiological costs associated with deposition of biliverdin pigments and because of their conspicuousness, eggs with blue-green coloration may reliably convey information about female or brood quality. We tested the hypothesis that expression of blue-green coloration of eastern bluebird (Sialia sialis) eggs positively correlates to female condition. First, we documented the incidence of egg color polymorphism within the population. We observed that 98% of females laid blue-green eggs while less than 2% laid white eggs and less than 1% laid pink eggs. In a subset of clutches, we used full spectrum reflectance spectrometry (300–700 nm) to compare eggshell coloration to measures of female condition. We found that the color of eggs within clutches was more similar than the color of eggs from different clutches, and that the blue-green eggs have spectral peaks that are consistent with the characteristic absorbance spectra of biliverdin pigmentation. Females in better body condition and older females laid more colorful eggs. Moreover, individual females laid more colorful eggs later in the laying sequence. Overall, these data indicate that egg coloration covaries with female condition, suggesting that egg coloration could function as a reliable signal of female quality or that egg coloration may allow females to recognize eggs laid by conspecific brood parasites.     

Male sexual attractiveness affects the investment of maternal resources into the eggs in peafowl (<Emphasis Type="Italic">Pavo cristatus</Emphasis>)

According to the differential investment hypothesis, females paired with attractive mates are expected to invest more in the current reproduction relative to females paired with unattractive males. We experimentally tested this hypothesis in the peafowl (Pavo cristatus) by providing females with males that differed in sexual attractiveness. In agreement with the differential allocation hypothesis, females paired with more ornamented males laid larger eggs, and deposited higher amounts of testosterone into the egg yolk, independently of the sex of the embryo. These results show that the association between paternal phenotype and offspring quality could arise via a differential maternal investment. They also suggest that, if ornamented males do transmit good genes to the progeny, the maternal differential investment can amplify the effect of such good genes on the offspring fitness.     

Are blue eggs a sexually selected signal of female collared flycatchers? A cross-fostering experiment

Impressive variation in egg colouration among birds has puzzled evolutionary biologists for a long time. The most frequently studied selective forces moulding egg colouration—predation and brood parasitism—have either received little empirical support or may play a role in only a minority of species. A novel hypothesis has suggested that egg colour may be significantly influenced by sexual selection. Females may deposit a blue-green pigment biliverdin into eggshells instead of using it for themselves as a powerful antioxidant. By this handicap, females may signal their quality to males, which are then hypothesized to increase their paternal effort. We experimentally tested the hypothesis in the collared flycatcher (Ficedula albicollis), a species laying blue-green eggs. We cross-fostered clutches between nests to disentangle effects of female/territory quality and egg colour on paternal effort and nestling quality. The results supported two assumptions of sexual signalling through egg colour hypothesis: Blue pigment seems to be a limited resource for females, and female quality is positively correlated with the intensity of the blue-green colour. However, we did not find support for the main prediction of the hypothesis, as male parental effort parameters (feeding frequencies to nestlings and intensity of nest defence) were unrelated to egg colour. We discuss possible reasons for the discrepancy between our results and previous correlative analyses that supported the hypothesis that blue egg colour may be a postmating, sexually selected signal in females.     

The effect of perceived female parasite load on post-copulatory male choice in a sex-role-reversed pipefish

The last several decades of research in behavioral ecology have resulted in a deeper appreciation of post-mating processes and sexual conflict in sexual selection. One of the most controversial aspects of sexual selection is cryptic mate choice. Here, we take advantage of male pregnancy in a sex-role-reversed pipefish (Syngnathus typhle) to quantify cryptic choice based on perceived parasite load and other sources of variance in female fitness. Studies have shown that S. typhle males preferentially mate with females with lower parasite loads and that a male’s perception of female parasite load can be altered by tattooing females. We manipulated the apparent parasite load of females in controlled mating experiments to test the hypothesis that post-copulatory sexual selection is dependent on a male’s perception of female parasite load in pipefish. Our results provided no evidence for cryptic male choice based on perceived female parasite load. However, we found evidence that eggs from larger females were more likely to result in viable offspring than eggs from smaller females and that the first female to mate with a male transferred more eggs per copulation on average. Overall, our results show that potential for post-copulatory sexual selection does exist in pipefish, but the male’s perception of female parasite load does not play a major role in this process.     

Sexual selection in a socially monogamous bird: male color predicts paternity success in the mountain bluebird, <Emphasis Type="Italic">Sialia currucoides</Emphasis>

Ornamental traits are thought to evolve because they give individuals an advantage in securing multiple mates. Thus, the presence of ornamentation among males in many monogamous bird species presents something of a conundrum. Under certain conditions, extra-pair paternity can increase the variance in reproductive success among males, thus increasing the potential for sexual selection to act. We addressed this possibility in the mountain bluebird (Sialia currucoides), a socially monogamous songbird in which males possess brilliant ultraviolet (UV)-blue plumage. Specifically, we asked whether a male’s success at siring offspring within his own nest and within the nests of other males was related to his coloration. In pairwise comparisons, males that sired extra-pair offspring were not more colorful than the males that they cuckolded. However, males that sired at least one extra-pair offspring were, on average, brighter and more UV-blue than males that did not sire extra-pair offspring. Brighter, more UV-blue males sired more offspring both with their own mate and tended to sire more offspring with extra-pair mates and thus sired more offspring overall. Our results support the hypothesis that the brilliant UV-blue ornamental plumage of male mountain bluebirds evolved at least in part because it provides males with an advantage in fertilizing the eggs of multiple females.     

Male lagoon gobies, <Emphasis Type="Italic">Knipowitschia panizzae</Emphasis>, prefer more ornamented to larger females

Female ornamentation may be directly sexually selected, by male choice or female competition, or occurs as the result of a genetic correlation, arising from sexual selection on males. However, increasing evidence supports the former hypothesis, suggesting that males actively choose their partner preferring traits indicative of female quality. In the lagoon goby, Knipowitschia panizzae, a polygynous species whose males perform parental care to eggs, body length and the size of a sex-specific yellow patch on the belly are known to be reliable indicators of female fecundity. In this paper, we tested, using dummies, the male’s mating preferences for female body and yellow belly patch sizes. The two experimental trials in which a single female trait was variable showed that males prefer a larger belly patch and a larger body size, indicating that both these characters are selected by male mate choice. However, when faced with dummies exhibiting an inverse combination of body and belly patch sizes (experiment 3), males significantly preferred the smaller ones with larger yellow belly patches. A calculation of dummy theoretical fecundity reveals that in the first two experiments, males would have received an immediate benefit from their choice in terms of egg number, whereas in the third one, males chose partners that would have provided them with fewer eggs. The male lagoon goby preference for females with larger belly patches, regardless of their size, suggests that this trait, in addition to indicating fecundity, conveys information about other aspects of female and/or egg quality.     

A field test of the intraspecific brood parasitism hypothesis in the golden egg bug (<Emphasis Type="Italic"> Phyllomorpha laciniata</Emphasis>)

In natural populations of golden egg bugs ( Phyllomorpha laciniata), females lay eggs on plants where they develop unattended, or on conspecifics, where they remain firmly glued until the nymphs hatch and start an independent life. Mortality rates among eggs laid on plants are higher than among eggs carried by adults. Because females cannot lay eggs on themselves, in order to improve offspring survival, they have to lay eggs on other individuals. Two hypotheses have been proposed to explain egg carrying: (1) the mating pair intraspecific brood parasitism hypothesis suggests that females dump eggs on copulating pairs, and (2) the paternal care hypothesis suggests that the system is driven mainly by males accepting eggs to improve the survival rates of their own offspring. Our data from the field show that 77% of the eggs are carried by males, because more males than females carry eggs, and because males carry a greater number of eggs. In addition, we show that mating males carry more recently laid eggs than single males. These results support the view that egg carrying is performed predominantly by males and that eggs are laid on males by their current mating partner, probably between repeated copulations. Males are likely to accept eggs, despite intermediate levels of paternity, because they cannot discriminate in favour of their own eggs, because rejected eggs will face 97% mortality rates on plants, and because they do not suffer mating costs when they carry eggs. However, females carry 23% of the eggs, but no differences in egg carrying have been found between mating and single females, suggesting that this is not the result of egg dumping while females are copulating. Egg carrying by females could reflect low levels of intraspecific parasitism, which is likely to reflect the low rate of successful attempts by egg-laying females who try to oviposit on other conspecifics rather indiscriminately, in an effort to improve the survival of their offspring.     

Brood defense and filial cannibalism in the spottail darter (<Emphasis Type="Italic">Etheostoma squamiceps)</Emphasis>: the effects of parental status and prior experience

Male spottail darters (Etheostoma squamiceps) defend nest sites in which females deposit eggs over the course of several weeks. In laboratory experiments, I tested three predictions of the hypothesis that the presence of eggs increases the value of a nest site to male spottail darters: (1) males should preferentially defend nests with eggs over empty nests, and males that sired the eggs should (2) spend more time defending them and (3) consume less of their broods than should alloparent males. Parent males were tested using eggs they were guarding in the field; alloparents included males that were not defending eggs immediately prior to the experiment (inexperienced), and males that were defending eggs in the field when captured but were given eggs sired by a different male (experienced). In choice experiments in which males were offered nest sites differing only in the presence of eggs, males preferred to defend nest sites with eggs regardless of parental status. Parent males spent significantly more time defending eggs and consumed less of their broods than did inexperienced alloparent males. Experienced alloparent males were similar to parent males in brood defense but had levels of filial cannibalism similar to inexperienced males, suggesting that prior experience may influence brood defense but not egg consumption.     

Spectral reflectance and communication in the wolf spider, <Emphasis Type="Italic">Schizocosa ocreata</Emphasis> (Hentz): simultaneous crypsis and background contrast in visual signals

Animal color patterns often reflect a compromise between natural selection for crypsis or inconspicuousness to predators and sexual selection for conspicuousness to potential mates. In leaf litter-dwelling wolf spider species like Schizocosa ocreata, body coloration often closely matches the background coloration of a generally brown environment. However, body parts used in communication should exhibit high contrast against background coloration. We used spectral analysis to examine male and female S. ocreata for matching and contrasting coloration against leaf litter. Values were plotted in multivariate color space, based on reflectivity in different frequency ranges. When viewed from above, colors of both males and females overlap with values for dead brown leaf litter and soil, suggesting cryptic coloration when viewed by potential predators. However, when viewed from a lateral perspective, both males and females show color values that are polar opposites of litter backgrounds, suggesting higher contrast when viewed by other spiders. Moreover, male secondary characters used in visual signaling by S. ocreata (tibia brushes) show the highest level of background contrast. These findings suggest that S. ocreata wolf spiders have color patterns that provide both crypsis and background contrast at the same time, depending on receiver viewing perspective.     

Are yolk androgens and carotenoids in barn swallow eggs related to parental quality?

Recently, evidence is mounting that females can adaptively engineer the quality of their offspring via the deposition of yolk compounds, including carotenoids and androgens. In this study, we simultaneously consider how both carotenoids and androgens in egg yolk relate to parental quality in barn swallows (Hirundo rustica erythrogaster). First, we found no relationship between concentrations or amounts of yolk androgens and carotenoids. Yolk carotenoids decreased with laying order, whereas we found no relationship between yolk androgens and laying order. Second, we tested the Investment Hypothesis, which predicts that high-quality females or females paired to high quality mates, allocate differentially more of these yolk compounds to their offspring. For carotenoids, we mostly found evidence to counter predictions of the Investment hypothesis: (1) Carotenoid concentrations varied among females, (2) heavier eggs contained lower carotenoid concentrations, although heavier yolks contained greater amounts of carotenoids, (3) eggs of earlier-laying females had lower concentrations in their eggs, and (4) yolk carotenoids were not correlated with clutch size or male plumage ornamentation. For androgens, we found weak support for the Investment Hypothesis: (1) Yolk androgens varied among females, (2) heavier eggs and yolks contained greater amounts, although not concentrations of androgens, (3) females paired to more colorful males laid eggs with greater concentrations of androgens, and (4) no effects of laying date or morphological correlates of female quality on androgen concentrations in egg yolks. Overall, these findings suggest that each yolk compound may have different functions and therefore may be regulated by different mechanisms.     

Biliverdin-based egg coloration is enhanced by carotenoid supplementation

Avian eggshell color is remarkably variable among and within species and its possible function has long been controversial. Female birds use biliverdin pigment to color their eggs blue and green. Although evidence is accumulating that blue-green eggshell coloration is costly to produce, the exact mechanisms underlying its expression are little studied. Biliverdin pigment is involved in important maintenance functions such as immune and antioxidant defenses and shows similar properties to carotenoid pigments. Carotenoids play a role as immunoenhancers and have the potential to ameliorate the impact of oxidative processes, although their antioxidant function could be minor for some bird species. Important life-history components can be limited by carotenoid availability, including sexual displays and fecundity. Here we explored if biliverdin-based eggshell pigmentation was affected by carotenoid availability in a seabird, by performing a carotenoid supplementation experiment in female blue-footed boobies (Sula nebouxii) after laying their first egg. In this species, blue eggshell color is associated with incubation patterns, and carotenoid availability affects the crucial trade-off between female foot ornamentation and fecundity. We found that under natural conditions, there was a decline in eggshell color with laying order, suggesting pigment limitation for females. However, carotenoid-supplemented females had enhanced second egg coloration compared to controls, and the color increase was independent of their previous pigment allocation to the first egg. Our results suggest that biliverdin-based eggshell coloration is costly to produce and can be alleviated by current carotenoid availability.     

Condition dependence of male display coloration in a jumping spider (Habronattus pyrrithrix)

In many animals, conspicuous coloration functions as a quality signal. Indicator models predict that such colors should be variable and condition dependent. In Habronattus pyrrithrix jumping spiders, females are inconspicuously colored, while males display brilliant red faces, green legs, and white pedipalps during courtship. We tested the predictions of the indicator model in a field study and found that male body condition was positively correlated with the size, hue, and red chroma of a male’s facial patch and negatively correlated with the brightness of his green legs. These traits were more condition dependent than non-display colors. We then tested a dietary mechanism for condition dependence using two experiments. To understand how juvenile diet affects the development of coloration, we reared juvenile spiders on high- and low-quality diets and measured coloration at maturity. To understand how adult diet affects the maintenance of coloration, we fed wild-caught adults with high- or low-quality diets and compared their coloration after 45 days. In the first experiment, males fed high-quality diet had redder faces, suggesting that condition dependence is mediated by juvenile diet. In the second experiment, red coloration did not differ between treatments, suggesting that adult diet is not important for maintaining the color after it is produced at maturity. Diet had no effect on green coloration in either experiment. Our results show different degrees of condition dependence for male display colors. Because red is dependent on juvenile diet, it may signal health or foraging ability. We discuss evidence that green coloration is age dependent and alternatives to indicator models for colorful displays in jumping spiders.     

Mate guarding in the swallowHirundo rustica

Summary The importance of mate guarding by males in the monogamous swallowHirundo rustica was studied by temporarily detaining the males. Mate guarding reduced the frequency of extra-pair copulations and of sexual chases involving female mates. Males participated in sexual chases more frequently if they had a non-fertile female. Neighbouring males of ‘widowed’ females increased their own mate guarding presumably in response to the experimentally increased rate of sexual chases. Neighbouring males with a fertile female increased their mate guarding more than did males with a non-fertile female. Addition of eggs to swallow nests in the post-fledging period of the first brood induced mate guarding by male nest owners. These males also copulated more frequently with their mates than did control males. Neighbouring male swallows responded to the increased mate guarding by showing sexual interest in the guarded females. removal of eggs from swallow nests during the laying period, leaving only one egg in the nest, resulted in reduced nest attendance by females. Male mates responded by increasing their mate guarding intensity as compared to controls, and neighbouring males showed an increased sexual interest in these females.     

The effect of male coloration on female mate choice in closely related Lake Victoria cichlids (Haplochromis nyererei complex)

We studied the effect of male coloration on interspecific female mate choice in two closely related species of haplochromine cichlids from Lake Victoria. The species differ primarily in male coloration. Males of one species are red, those of the other are blue. We recorded the behavioral responses of females to males of both species in paired male trials under white light and under monochromatic light, under which the interspecific differences in coloration were masked. Females of both species exhibited species-assortative mate choice when colour differences were visible, but chose non-assortatively when colour differences were masked by light conditions. Neither male behaviour nor overall female response frequencies differed between light treatments. That female preferences could be altered by manipulating the perceived colour pattern implies that the colour itself is used in interspecific mate choice, rather than other characters. Hence, male coloration in haplochromine cichlids does underlie sexual selection by direct mate choice, involving the capacity for individual assessment of potential mates by the female. Females of both species responded more frequently to blue males under monochromatic light. Blue males were larger and displayed more than red males. This implies a hierarchy of choice criteria. Females may use male display rates, size, or both when colour is unavailable. Where available, colour has gained dominance over other criteria. This may explain rapid speciation by sexual selection on male coloration, as proposed in a recent mathematical model. Received: 11 April 1997 / Accepted after revision: 27 July 1997     

Robin’s egg blue: does egg color influence male parental care?

A recent hypothesis suggests that birds’ blue-green egg colors may be a sexually selected signal of female (and potentially nestling) quality that males use to make parental investment decisions. While there is some empirical support for this idea, both theory and observations question its validity. To test this hypothesis experimentally, we examined the influence of egg color on male American robin Turdus migratorius behavior by replacing natural clutches with four artificial eggs that were all either pale or vividly colored, close to the extremes in natural egg coloration. At the end of the incubation period, three unrelated nestlings were fostered into each experimental nest, and parental provisioning behavior was monitored when nestlings were 3, 6, and 9 days old. Male provisioning rate for 3-day-old nestlings was significantly higher in the vivid egg treatment compared to both the pale egg treatment and untreated controls, but there was no effect of egg color on paternal behavior at the older nestling stages. Male feeding rate at unmanipulated nests was only weakly positively related to natural egg color (chroma) when nestlings were 3 days old. These results suggest that blue-green egg color may act as a post-mating signal of female quality or investment in this species, but our findings do not exclude the possibility that egg color pigmentation also serves other adaptive functions.     

Direct male-male competition can facilitate invasion of new colour types in Lake Victoria cichlids

The possibility that disruptive sexual selection alone can cause sympatric speciation is currently a subject of much debate. The initial difficulty for new and rare ornament phenotypes to invade a population, and the stabilisation of the resulting polymorphism in trait and preference make this hypothesis problematic. Recent theoretical work indicates that the invasion is facilitated if males with the new phenotype have an initial advantage in male-male competition. We studied a pair of sympatric incipient species of cichlids from Lake Victoria, in which the red (Pundamilia nyererei) and blue males (P. pundamilia) vigorously defend territories. Other studies suggested that red phenotypes may have repeatedly invaded blue populations in independent episodes of speciation. We hypothesised that red coloration confers an advantage in male-male competition, assisting red phenotypes to invade. To test this hypothesis, we staged contests between red and blue males from a population where the phenotypes are interbreeding morphs or incipient species. We staged contests under both white and green light condition. Green light effectively masks the difference between red and blue coloration. Red males dominated blue males under white light, but their competitive advantage was significantly diminished under green light. Contests were shorter when colour differences were visible. Experience of blue males with red males did not affect the outcome of a contest. The advantage of red over blue in combats may assist the red phenotype to invade blue populations. The apparently stable co-existence of red and blue incipient species in many populations of Lake Victoria cichlids is discussed.Communicated by C. St. Mary     

Male-male competition ensures honest signaling of male parental ability in the three-spined stickleback (Gasterosteus aculeatus)

The importance of socially imposed costs for the evolution and maintenance of honest sexual signals has received less attention than other costs. Here I show that male-male competition can increase the honesty of sexual signaling in relation to male parental ability in a species with flexible signaling. When four three-spined stickleback (Gasterosteus aculeatus) males were allowed to court a female first separately and then in competition, red nuptial coloration under competition reflected male parental ability more accurately than red coloration when separated. Parental ability was determined as the ability of the male to raise a clutch of eggs to the hatching stage under interaction with other breeding and non-breeding males. The increased honesty under competition was probably due to subordinate males of poor parental ability decreasing their color expression under interaction to reduce the risk of fights with superior males. However, socially imposed costs of signaling were probably not the main factors maintaining honest signaling, as red coloration reflected male parental ability also in the absence of competition, although less accurately. Nevertheless, the small-scale differences that male-male competition induced can significantly facilitate adaptive female choice and have large impacts on sexual selection. Received: 7 July 2000 / Revised: 31 August 2000 / Accepted: 4 September 2000     

Carotenoid-derived ornaments reflect parental quality in male and female yellow-eyed penguins (<Emphasis Type="Italic">Megadyptes antipodes</Emphasis>)

The handicap principle suggests that ornamental traits that function as honest signals in mate selection must be costly to be effective. We evaluated in the sexually monochromatic yellow-eyed penguin (Megadyptes antipodes) whether the carotenoid-derived plumage and eye coloration predicts parental quality and whether males and females within pairs mate assortatively in relation to these carotenoid-derived ornaments. In addition, we investigated whether age or body condition was related to the coloration of the ornamental traits. In yellow-eyed penguins, parental quality of males and females was predicted by eye and head plumage coloration. Even when we controlled for gender- and age-specific differences, eye and head plumage coloration reflected honestly parental quality. Males and females mated assortatively in relation to these ornamental traits. While age influenced coloration of both the eye and head plumage, body condition was related only to the saturation of plumage coloration. These results provide evidence that the carotenoid-derived ornaments in yellow-eyed penguins reflect the parental abilities of birds and, therefore, may be costly signals. Potentially, female and male yellow-eyed penguins could use eye and plumage coloration as an indirect cue in assessing age and quality of individual birds during mate choice. This is only the second study to examine plumage coloration in relation to sexual selection in penguins, while conspicuous ornamental traits in other species of penguin beg the question whether they also play a role in sexual selection.Electronic Supplementary Material Supplementary material is available in the online version of this article at Communicated by C.R. Brown