MALE MATE CHOICE AND THE EVOLUTION OF FEMALE PLUMAGE COLORATION IN THE HOUSE FINCH

The house finch (Carpodacus mexicanus) is a sexually dichromatic passerine in which males display colorful plumage and females are generally drab brown. Some females, however, have a subdued version of the same pattern of ornamental coloration seen in males. In previous research, I found that female house finches use male coloration as an important criterion when choosing mates and that the plumage brightness of males is a reliable indicator of male nest attentiveness. Male house finches invest substantially in the care of young and, like females, stand to gain by choosing high-quality mates. I therefore hypothesized that a female's plumage brightness might be correlated with her quality and be the basis for male mate choice. In laboratory mate choice experiments, male house finches showed a significant preference for the most brightly plumaged females presented. Observations of a wild population of house finches, however, suggest that female age is the primary criterion in male choice and that female plumage coloration is a secondary criterion. In addition, yearling females tended to have more brightly colored plumage than older females, and there was no relationship between female plumage coloration and overwinter survival, reproductive success, or condition. These observations fail to support the idea that female plumage coloration is an indicator of individual quality. Male mate choice for brightly plumaged females may have evolved as a correlated response to selection on females to choose brightly colored males.     

Does part reproductive history predict competitive interactions and male mating success in pupfish?

Two experiments were performed to determine the effect of past territoriality and mating success on subsequent dominance and ability to attract females. First, in 14 staged, pair-wise encounters, the development of nuptial coloration and agonistic behaviour was examined in two types of males: previously territorial (PT) and previously non-territorial (PNT) males. Previously territorial males developed a more intense nuptial coloration and won all contests. Second, to test the males' ability to attract females, other factors were controlled that could have affected female mate choice, such as male size, quality of breeding substrate and male-male interactions. In 40 trials, PT males were more active, developed a more intense nuptial coloration, courted females more vigorously, spawned sooner and had a higher mating success than PNT males. Thus, in pupfish, Cyprinodon pecosensis, previous reproductive history is a good indicator of both dominance and mating success. Only males in good physical condition achieve high mating success, and both intra- and inter-sexual selection are important in maintaining the close correlation between expression of nuptial coloration, a second sexual trait, and other male attributes, such as physical condition and vigour, that allow a male to secure and defend a territory against rivals and to attract and spawn with females.     

Effect of mating on survival at low temperature in females of the Japanese common grass yellow,Eurema mandarina

1. In some insects that overwinter as adults, mating occurs both before and after overwintering. Two hypotheses have been proposed to explain the adaptive significance of pre‐overwintering copulation of females. One is the bet‐hedging hypothesis, which explains pre‐overwintering copulation as a preparation for less chance of mating in the following spring. The other is the nuptial gift hypothesis, which states that secretions derived from males increase overwintering success of females. 2. In Eurema mandarina, both diapause autumn‐ and non‐diapause summer‐form male adults emerge with autumn‐form female adults in the last generation in a year. Most autumn‐form females mate with summer‐form males before winter, and re‐mate with autumn‐form males in the following spring. Because autumn‐form females have sufficient chances for mating after overwintering, the nuptial gift hypothesis has been regarded as the more probable hypothesis. 3. To test the nuptial gift hypothesis, the survival period was compared under short‐day conditions at 10 °C between mated and unmated females that had been reared on sucrose solution at 25 °C for 15–21 days. The mated females had significantly greater longevity than the unmated females, supporting the nuptial gift hypothesis. Body size also affected the survival period. 4. The results suggest that the nuptial gift is an important factor for the evolution of pre‐overwintering copulation in species in which females mate both before and after overwintering.     

Do Female Mandrills Prefer Brightly Colored Males?

Although secondary sexual adornments are widespread in male primates, few studies have examined female choice for these characters. Mandrills (Mandrillus sphinx) present an extreme example of sexual dimorphism, with males exhibiting an array of striking adornments. The most dominant adult male in a group exhibits the brightest and most extensive red coloration, while the other males are less brightly colored. I examined whether female mandrills prefer brightly colored males using data on periovulatory sexual behavior during the 1996 mating season for all males 8 years old (n = 5) and all parous females (n = 9) in a semifree-ranging colony at CIRMF, Gabon. Brightness of male coloration is significantly positively correlated with time spent within 2 m of females, female responsibility for proximity, number of sexual presentations received, % approaches accepted by females, and % inspections with which females cooperated. Females also groomed only the brightest male. Behaviors indicating female preference are not correlated significantly with male dominance rank, and partial correlations confirm that the influence of male color on female behavior is stronger than that of male rank. With the influence of male dominance rank controlled, correlation coefficients between female behaviors and male mating success are high and positive. In further support of the hypothesis that females show mate choice for brightly colored males, independent of dominance rank, I report an unusual case wherein the alpha male fell in rank without loss of coloration. He experienced no significant change in female responsibility for proximity, sexual presentations received, or female reaction to approaches or inspections, though he was no longer observed to mate. Accordingly, female mandrills attend to differences in male secondary sexual characters and favor brightly colored males. As brightly colored males are also dominant this reinforces the influence of male-male competition on male reproductive success and may explain the very high reproductive skew in mandrill males and their extraordinary appearance.     

The Disruption Hypothesis Does Not Explain Mate‐Choice Copying in the Guppy (Poecilia reticulata)

In some species, female mate choice is non‐independent as, under certain circumstances, females may copy the mate choice of other nearby females. One standard experimental protocol used to test for mate‐choice copying is the mate‐choice ‘reversal’ protocol. In this protocol, a focal female is allowed to choose between two males as potential mates and then is presented with an opportunity to see another female (i.e. the model female) choose the male that she did not initially choose. The focal is subsequently allowed to again choose between the same set of males. An observed reversal of her initial choice in this second preference test has been previously interpreted as evidence for mate‐choice copying. Alternatively, it has recently been proposed that environmental events, such as seeing the mate choice of nearby females that occur within the visual field of a female actively engaged in mate assessment, may ‘disrupt’ her decision‐making behavior and consequently alter the consistency of her mating preference, and may thus cause mate‐choice reversals. The disruption hypothesis predicts that if a model female is placed near the male that the focal female initially chose, the latter's mate preference would be disrupted and she would subsequently and consistently prefer the male that she initially rejected. Here we examined whether the disruption hypothesis explains mate‐choice copying in the guppy (Poecilia reticulata). Our results do not support this hypothesis, but rather provide further support for mate‐choice copying in the guppy.     

Coloration,Paternity, and Assortative Mating in Western Bluebirds

Coloration in birds can act as an important sexual signal in males, yet in many species, both sexes display bright colors. Social selection may account for this pattern, with more brightly colored individuals pairing together on the best territories. Mutual mate choice may also explain this, as males investing a great deal of parental care in the offspring should be choosy about their social mates. It is less clear whether this pattern of mate choice can apply to extra‐pair partners as well. We examined western bluebirds (Sialia mexicana) to determine whether more colorful individuals tended to pair with one another, both in social pairs and between females and their extra‐pair partners. Both male and female western bluebirds display both UV‐blue structural plumage and a melanin‐based chestnut breast patch, although females are duller than males. Social pairs mated assortatively with regard to UV‐blue brightness, but not chestnut coloration. There was no evidence that extra‐pair partners mated assortatively, but males with brighter UV‐blue coloration had fewer extra‐pair offspring in their nests. Older males were more successful at siring extra‐pair offspring, despite displaying no differences in coloration compared to younger males. Coloration did not play a role in determining extra‐pair male success. These results suggest that coloration plays a role in the formation of social pairs, but not mate choice for extra‐pair partners.     

Black Male Bellies and Red Female Throats: Color Changes with Breeding Status in a Threespine Stickleback

This paper provides the first report of black nuptial coloration on the ventral side for a population of threespine sticklebacks, Gasterosteus aculeatus, in Northern California. Black nuptial coloration was least intense during precourtship. Although the black coloration intensified during courtship, it was not a significant predictor of female choice and, unlike the red throat and blue eyes, was not inversely correlated with the number of female introductions necessary before spawning occurred. Black coloration was the most intense for males who successfully hatched embryos, supporting a parental-defense role late in the cycle. Unsuccessful fathers had more intensely colored red throats, blue eyes, and black bellies during most of the reproductive cycle than successful fathers. Some females in this study developed red coloration on their throat, although none to the intensity or distribution typical of a breeding male.     

Interspecific mate choice by late-courting male western grebes

In mixed populations of western and Clark's grebes, advertisingcalls by males and females play a critical role in mate choiceand reproductive isolation. We conducted field playback experimentsthat tested whether courting western grebe males became lesschoosy in their responses to female Clark's grebe calls as themating season progressed and mating opportunities diminished.Late-courting western grebe males were much more likely to answerand approach advertising calls of Dark's grebe females thanwere males courting earlier in the season. This change in responsivenessoccurred as the operational sex ratio index of the populationapproached 3:1 male calls per female call. These and field censusdata support the hypothesis that late-season hybridization betweenthese two closely related species may be a result not of speciesmisidentification, but of active and adaptive mate choice byindividuals with limited alternatives.     

Blue structural coloration of male eastern bluebirds Sialia sialis predicts incubation provisioning to females

Plumage coloration has been suggested to serve as an honest signal of benefits that males provide to females. One benefit proposed for females that choose to mate with elaborately colored males is that such males might provide more food resources to the females. To test this hypothesis, we investigated the relationship between the rates at which males provisioned incubating females and the structural ultraviolet (UV)/blue coloration and melanin-based chestnut coloration of male eastern bluebirds Sialia sialis , a sexually dichromatic songbird in which coloration has been shown to be sexually selected in males. We found that males with brighter UV/blue coloration provisioned incubating females more often than did drabber males. Melanin coloration, however, was not correlated with provisioning rates. Moreover, provisioning rates were correlated with the length of time that females spent off the nest, indicating an important benefit of increased male provisioning. These data support the hypothesis that female bluebirds receive direct resource benefits by pairing with males with bright structural coloration.     

Male coloration signals direct benefits in the European bitterling (Rhodeus amarus)

Female mating preferences are frequently associated with exaggerated male sexual traits. In the European bitterling, Rhodeus amarus, a fish with a resource-based mating system, male coloration is not associated with indirect genetic benefits of female mate choice, and does not reliably signal spawning site quality. We tested a link between the extent of male carotenoid-based coloration and testis size and number of spermatozoa stripped from the testes. Male body size predicted spermatozoa number, but less reliably than the extent of male coloration. Male color was a highly significant predictor of spermatozoa number, with approximately 26 % of variance in the number of spermatozoa stripped from males predicted from male color after controlling for male body size. Body size, but not coloration, predicted teste size. Female bitterling often risk sperm limitation, especially during pair spawnings, and male nuptial coloration may be under direct selection through female mate choice as a signal of male fertilization efficiency.     

Ultraviolet nuptial colour determines fight success in male European green lizards (Lacerta viridis)

Animal communication through colour signals is a central theme in sexual selection. Structural colours can be just as costly and honest signals as pigment-based colours. Ultraviolet (UV) is a structural colour that can be important both in intrasexual competition and mate choice. However, it is still unknown if a UV signal alone can determine the outcome of male-male fights. European green lizard (Lacerta viridis) males develop a nuptial throat coloration with a strong UV component. Among males differing only in their manipulated UV colour, females prefer males with higher UV. Here, we experimentally decreased the UV coloration of randomly chosen males from otherwise similar male pairs to test the hypothesis that a difference in UV colour alone can affect fight success during male-male competition. Our results fully supported the hypotheses: in almost 90 per cent of the contests the male with reduced UV lost the fight. Our results show that UV can be an important signal, affecting both female mate choice and determining male fight success.     

Aggressive Behavior and Courtship Rejection in Brightly and Plainly Colored Female Keeled Earless Lizards (Holbrookia propinqua)

Relationships between bright secondary sexual coloration and behavior were studied in female Holbrookia propinqua, which develop striking orange and yellow colors during the breeding season. In tethered introduction studies, brightly colored females performed aggressive courtship rejection behaviors toward conspecific males; plainly colored females were not aggressive toward males, but attempted to avoid them. Responses of females of the two color patterns toward conspecific females of both color phases were not detectably different. Experimental introductions of lizards with coloration modified by paint showed that females of both color patterns recognize any other lizard bearing the bright female colors as female, regardless of actual sex. Both the orange and yellow components were shown to contribute to sex recognition. The yellow component alone allowed accurate sex identification, but only half the females responded to males painted with only the orange female component as if they were females. Because females did not behave differently toward other females on the basis of coloration, the hypothesis that bright coloration evolved as an adaptive signal between females is rejected. The dark ventrolateral stripes of male and plainly colored females did not appear to affect intraspecific social responses by females.     

Fitness correlates of male coloration in a Lake Victoria cichlid fish

Sexual selection by female choice has contributed to the rapidevolution of phenotypic diversity in the cichlid fish speciesflocks of East Africa. Yet, very little is known about the ecologicalmechanisms that drive the evolution of female mating preferences.We studied fitness correlates of male nuptial coloration ina member of a diverse Lake Victoria cichlid lineage, Pundamilianyererei. In this species, male red coloration is subject tointraspecific sexual selection by female mate choice. Male nuptialcoloration plays a critical role also in reproductive isolationbetween this species and the closely related sympatric speciesP. pundamilia. Here, we show that P. nyererei male colorationis carotenoid based, illustrating the potential for honest signalingof individual quality. In a wild population, we found that variationin male coloration was not associated with variation in a setof strongly intercorrelated indicators of male dominance: malesize, territory size, and territory location. Instead, the 2male characters that predominantly determine female choice,territory size and red coloration, may be independent predictorsof male quality: males with bright red coloration and largeterritories had lower parasite infestation rates. As a result,female preferences tended to select against heavily parasitizedmales. Consistent with parasite-mediated sexual selection, maleshad higher and more variable parasite loads than females.     

Diet affects female mating behaviour in a seed‐feeding beetle

In species where males provide nuptial gifts, females can improve their nutritional status and thus increase their fecundity by mating when in need of resources. However, mating can be costly, so females should only mate to acquire resources when the need for resources is large, such as when females are nutritionally‐deprived. Two populations of the seed‐feeding beetle Callosobruchus maculatus, a species that produces relatively large nuptial gifts, are used to test whether female nutritional status affects mating behaviour. Female access to water, sugar and yeast are manipulated and the fitness consequences of these manipulations are examined together with the effects of diet on the propensity of nonvirgin females to mate. Access to water has a small but significant effect on mass loss over time, lifespan and fecundity of females, relative to unfed controls. Access to sugar (dissolved in water) improves female fecundity and lifespan above that of hydrated females but access to yeast has no positive effects on female survival or reproduction. Diet has a large effect on both receptivity of nonvirgin females to a male and how quickly they accept that male. Unfed females are both more likely to mate, and accept a mate more quickly, than females provided access to water, which are more likely to mate and accept a mate more quickly than females provided with sugar. This rank order of behaviours matches the order predicted if females increase their mating rate when nutritionally deprived (i.e. it matches the effect of diet on female fitness). The results obtained also suggest that mate choice may be condition‐dependent: females from one population (Burkina Faso) show a preference for large males when well‐fed but not when unfed, although this result is not found in a second population (South India). It is concluded that nutritionally‐deprived females are more receptive to mates than are well‐fed females, consistent with the hypothesis that females ‘forage’ for nuptial gifts, or at least more willingly accept sperm in exchange for nuptial gifts, when they are nutritionally deprived.     

Color patterns and species recognition in four closely related species of Lake Malawi cichlid

We examined interspecific female mating preferences in fourclosely related species of cichlid belonging to the Pseudotropheuszebra species complex of Lake Malawi. These species differin coloration but are similar in other respects, suggestingthat male color patterns may be important to female mate choicein species recognition. To test this hypothesis, we presented females from each species with a choice of four males, one ofher own species and three others that were each of a differentspecies. We also gave each female a choice between the threeheterospecific males only. In all four species, females showeda significant preference for conspecific males in the four-waychoice and chose the male with the most similar color patternto the conspecific male in the three-way choice. These resultsare discussed with reference to the theory of sexual selectionon color patterns as a means of sympatric speciation in cichlids.     

Does Female Personality Determine Mate Choice Through Sexual Cannibalism?

Animal personalities (e.g. consistent across‐context behavioural differences between individuals) can lead to differences in mate choice. However, evidence for this link remains limited. Pre‐mating sexual cannibalism can be a behavioural syndrome (i.e. a suboptimal personality) in which adaptive female aggression towards heterospecific prey spills over on non‐adaptive aggression towards courting males, independently of the female mating or feeding status (i.e. the ‘aggressive spillover hypothesis’, ASH). On the other hand, sexual cannibalism can also be a form of mate choice by which females selectively kill or mate with males depending on the male phenotype. We introduce the hypothesis that the most aggressive females in the population will not only attack males more frequently, but will be less likely to impose sexual selection on males through sexual cannibalism. Assuming that in a field common garden experiment in which females were fed ad libitum the rate of weight gain by a female may reflect her voracity or aggressiveness, we show that in the cannibalistic burrowing wolf spider Lycosa hispanica (formerly L. tarantula), voracity towards heterospecific prey predicts a female's tendency towards sexual cannibalism. Unmated females with higher weight gains were more cannibalistic and attacked males regardless of the male phenotype. On the other hand, females that were less voracious tended to be less cannibalistic, and when they did kill a male, they were selective, killing males in poorer condition and mating with those in better condition. Our results demonstrate that females with different phenotypes (growth rates) differently imposed selection on male condition, tentatively supporting the hypothesis that female aggression levels can spill over on sexual selection through sexual cannibalism.     

INTEGRATING PHYLOGENY AND EXPERIMENTAL ETHOLOGY: FROM PATTERN TO PROCEs

Phylogenetic systematics offers ethologists a method for uncovering macroevolutionary patterns of behavioral diversity, which can be used to generate predictions for experimental investigation of microevolutionary processes. I used phylogenetic methods to disentangle the contributions of various selection pressures in the evolution of sexually dimorphic nuptial coloration in gasterosteid fishes in general, and Gasterosteus aculeatus in particular. Based upon the phylogenetic relationships between breeding colors and breeding behaviors in the gasterosteids, three predictions relevant to a discussion of nuptial coloration in G. aculeatus were proposed. The origin and elaboration of nuptial coloration was (1) weakly associated with male/male interactions (intrasexual selection), (2) moderately associated with parental care (natural selection) and (3) strongly associated with male/female interactions (intersexual selection). I tested the hypothesized macroevolutionary relationships between male breeding color and behavior in two sets of experiments studying changes in male nuptial coloration across the breeding cycle and female choice based on intensity of male color. The results of these experiments at the microevolutionary level of analysis corroborated the macroevolutionary predictions and confirmed the original intuition of previous researchers: male body color intensity is an important component of female mate choice in G. aculeatus. This study demonstrates that a phylogenetic hypothesis can generate predictions that are experimentally testable and falsifiable.     

How Do Females’ Genetic Characteristics Influence Male Mate Preference in the Terrestrial Isopod Armadillidium vulgare?

Genetic diversity is a key factor that can influence mate choice in many species. We experimentally determined the influence of this factor on mate preference in the crustacean terrestrial isopod Armadillidium vulgare. This biological model is gregarious which could increase the risk of inbreeding by mating with closely related partners. Mechanisms of inbreeding avoidance during mate choice can thus be expected. Moreover, previous studies predict that males would be the choosy sex. We performed Y‐choice tests giving males the choice between two females presenting different levels of heterozygosity and genetic similarity to the male. Our results show potential inbreeding avoidance according to the genetic characteristics of females presented to males. The higher the variation in genetic similarity to the male between females is, the higher the preference of the male towards the most dissimilar female is. Hence, male preferences may only be detectable when the difference between females’ genetic characteristics is large enough. If heterozygosity is associated with fitness in A. vulgare (as in many organisms), the patterns of mate preference we observe may be adaptive.     

Female mating preferences and male coloration covary with water transparency in a Lake Victoria cichlid fish

Rapid speciation in Lake Victoria cichlid fish of the genus Pundamilia may be facilitated by sexual selection: female mate choice exerts sexual selection on male nuptial coloration within species and maintains reproductive isolation between species. However, declining water transparency coincides with increasingly dull coloration and increasing hybridization. In the present study, we investigated the mechanism underlying this pattern in Pundamilia nyererei, a species that interbreeds with a sister species in turbid but not in clear water. We compared measures of intraspecific sexual selection between two populations from locations that differ in water transparency. First, in laboratory mate‐choice experiments, conducted in clear water and under broad‐spectrum illumination, we found that females originating from turbid water have significantly weaker preferences for male coloration than females originating from clear water. Second, both the hue and body coverage of male coloration differ between populations, which is consistent with adaptation to different photic habitats. These findings suggest that the observed relationship between male coloration and water transparency is not mediated by environmental variation alone. Rather, female mating preferences are indicated to have changed in response to this variation, constituting the first evidence for intraspecific preference‐trait co‐evolution in cichlid fish. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 398–406.     

No evidence for an indirect benefit from female mate preference in Arctic charr Salvelinus alpinus,but female ornamentation decreases offspring viability

Female mate choice is considered an important evolutionary agent, but there has been an ongoing debate over the fitness consequences it produces, especially in species that have a resource‐free mating system. We examined a potential fitness benefit resulting from the pre‐spawning mate preference in Arctic charr Salvelinus alpinus, a salmonid fish with no parental care. The females were first allowed to discriminate behaviourally between two males presented to them in a free choice test. We then tested with controlled fertilizations whether the females would accrue indirect genetic benefits for their offspring, as measured by embryonic viability, if they had mated with the male they preferred. Both parental identities influenced offspring survivorship, but the females did not consistently prefer the male which gave her the higher reproductive success. Neither was the degree of male red breeding coloration associated with female preference or the observable genetic quality. In contrast, there was a negative relationship between female coloration and her offspring survivorship, suggesting a significant trade‐off in resource investment between sexual ornamentation and reproduction. To conclude, the potential indirect fitness consequences arising from females' pre‐spawning mate preference seem to be negligible in early stages of development of Arctic charr. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 602–611.