Familiarity adds to attractiveness in matters of siskin mate choice

There is currently considerable controversy in evolutionary ecology revolving around whether social familiarity brings attraction when a female chooses a mate. The topic of familiarity is significant because by avoiding or preferring familiar individuals as mates, the potential for local adaptation may be reduced or favoured. The topic becomes even more interesting if we simultaneously analyse preferences for familiarity and sexual ornaments, because when familiarity influences female mating preferences, this could very significantly affect the strength of sexual selection on male ornamentation. Here, we have used mate-choice experiments in siskins Carduelis spinus to analyse how familiarity and patterns of ornamentation (i.e. the size of wing patches) interact to influence mating success. Our results show that females clearly prefer familiar individuals when choosing between familiar and unfamiliar males with similar-sized wing patches. Furthermore, when females were given the choice between a highly ornamented unfamiliar male and a less ornamented familiar male, half of the females still preferred the socially familiar birds as mates. Our finding suggests that male familiarity may be as important as sexual ornaments in affecting female behaviour in mate choice. Given that the potential for local adaptation may be favoured by preferring familiar individuals as mates, social familiarity as a mate-choice criterion may become a potential area of fruitful research on sympatric speciation processes.     

Ejaculate investment and attractiveness in the stalk‐eyed fly,Diasemopsis meigenii

The phenotype‐linked fertility hypothesis proposes that male fertility is advertised via phenotypic signals, explaining female preference for highly sexually ornamented males. An alternative view is that highly attractive males constrain their ejaculate allocation per mating so as to participate in a greater number of matings. Males are also expected to bias their ejaculate allocation to the most fecund females. We test these hypotheses in the African stalk‐eyed fly, Diasemopsis meigenii. We ask how male ejaculate allocation strategy is influenced by male eyespan and female size. Despite large eyespan males having larger internal reproductive organs, we found no association between male eyespan and spermatophore size or sperm number, lending no support to the phenotype‐linked fertility hypothesis. However, males mated for longer and transferred more sperm to large females. As female size was positively correlated with fecundity, this suggests that males gain a selective advantage by investing more in large females. Given these findings, we consider how female mate preference for large male eyespan can be adaptive despite the lack of obvious direct benefits.     

Does male-biased predation lead to male scarcity in viviparous fish?

Male predation risk due to ornaments seldom reduces female mating opportunities because males escape costs through alternative mating strategies and/or females cease to select for highly ornamented males. Males of the Amarillo fish Girardinichthys multiradiatus (Goodeidae) have large sexually selected fins that impair attack-avoidance manoeuvres. This fish was used to seek evidence that intersexual selection for handicapping traits can result in a deficit of acceptable mating partners. Also it was examined whether, under male scarcity, females remain choosy to the point of missing mating opportunities, and that they can exert effective control over matings, which is a pre-condition of effective female choice. It was found that snakes prey disproportionately on males, that it leads to female-biased sex ratios, and that highly ornamented males are more scarce after predation than males with small ornaments. Females can avoid being fertilized by unattractive males, and that missing one reproductive period can lead to infertility. Thus it appears that females have promoted the exaggeration of a male trait that increases predation risk, remain choosy even when acceptable males are scarce, and pay a large cost when missing mating opportunities. A prediction from these results is that females enjoy substantial fitness benefits from mating with highly ornamented males, which override the occasional fatal costs of refusing to mate with sub–optimal males. One potential consequence of female selectivity and control over matings when males are scarce may be a reduced capability to colonize new habitats.     

Production of plumage ornaments among males and females of two closely related tropical passerine bird species

The evolution of elaborate secondary sexual traits (i.e., ornaments) is well‐studied in males but less so in females. Similarity in the appearance of ornaments between males and females supports the view that female ornaments arise as a neutral byproduct of selection on male traits due to genetic correlation between sexes, but recent research suggests an adaptive function of female ornaments in at least some contexts. Information on the degree to which production of ornaments differs between the sexes can shed light on these alternative perspectives. We therefore characterized the structural underpinnings of melanin‐based plumage production in males and females of two closely related passerine bird species (genus Malurus). Importantly, both ornamented and unornamented phenotypes in each sex are present between these two species, providing an opportunity to test the null expectation of equivalent modes of production in male and female ornamented phenotypes. In Malurus alboscapulatus, ornamented females are qualitatively similar to males, but we describe a distinctive ornamented female phenotype that differs from that of males in lacking a blue sheen and in lower feather barbule density. In M. melanocephalus, unornamented males and females are also similar in appearance, and we describe a similarity between unornamented phenotypes of males and females in both color and underlying feather barbule structure and pigment composition. Unornamented male M. melanocephalus can flexibly transition to the ornamented phenotype in weeks, and we found extreme differences in color and feather structure between these two alternative male phenotypes. These results contradict the idea that female ornaments have evolved in this system following a simple switch to male‐like plumage by demonstrating greater complexity in the production of the ornamented phenotype in males than in females.     

Age and experience affect female choice in the guppy (Poecilia reticulata)

Female choices of males, and how these choices are influenced by ecological and social factors, have been studied extensively. However, little is known about the effects of age and breeding experience on female mating decisions. We used video techniques to examine female mate choice in guppies based on the area of carotenoid (orange) pigmentation on the body. Females were presented with paired images of males, one ornamented and the other plain. Visual preference for each male was measured. Age-related changes in the criteria of choice were examined by comparing the responses of the same mature but sexually inexperienced 6-mo-old and 12-mo-old females. Effects of breeding experience on female choice were examined by comparing mate preferences of 12-mo-old female virgins with their preferences after they had mated and produced a brood. Female preferences for ornamented males with large areas of carotenoid pigment changed with age but not with mating experience. Six-month-old virgin females preferred ornamented males, whereas 12-mo-old virgin and postpartum females did not differentiate between males based on orange coloration. The results are discussed in light of life-history theory and have important implications for studies of sexual selection as well as for the design of mate-choice studies.     

Independent Mating Preferences for Male Body Size and Coloration in Female Trinidadian Guppies

Although females in numerous species generally prefer males with larger, brighter and more elaborate sexual traits, there is nonetheless considerable intra‐ and interpopulation variation in mating preferences amongst females that requires explanation. Such variation exists in the Trinidadian guppy, Poecilia reticulata, an important model organism for the study of sexual selection and mate choice. While female guppies tend to prefer more ornamented males as mates, particularly those with greater amounts of orange coloration, there remains variation both in male traits and female mating preferences within and between populations. Male body size is another trait that is sexually selected through female mate choice in some species, but has not been examined as extensively as body coloration in the guppy despite known intra‐ and interpopulation variation in this trait among adult males and its importance for survivorship in this species. In this study, we used a dichotomous‐choice test to quantify the mating preferences of female guppies, originating from a low‐predation population in Trinidad, for two male traits, body length and area of the body covered with orange and black pigmentation, independently of each other. We expected strong female mating preferences for both male body length and coloration in this population, given relaxation from predation and presumably relatively low cost of choice. Females indeed exhibited a strong preference for larger males as expected, but surprisingly a weaker (but nonetheless significant) preference for orange and black coloration. Interestingly, larger females demonstrated stronger preferences for larger males than did smaller females, which could potentially lead to size‐assortative mating in nature.     

Can non‐directional male mating preferences facilitate honest female ornamentation?

Recent studies have demonstrated male mate choice for female ornaments in species without sex-role reversal. Despite these empirical findings, little is known about the adaptive dynamics of female signalling, in particular the evolution of male mating preferences. The evolution of traits that signal mate quality is more complex in females than in males because females usually provide the bulk of resources for the developing offspring. Here, we investigate the evolution of male mating preferences using a mathematical model which: (i) specifically accounts for the fact that females must trade-off resources invested in ornaments with reproduction; and (ii) allows male mating preferences to evolve a non-directional shape. The optimal adaptive strategy for males is to develop stabilizing mating preferences for female display traits to avoid females that either invests too many or too few resources in ornamentation. However, the evolutionary stability of this prediction is dependent upon the level of error made by females when allocating resources to either signal or fecundity.     

Correlates of male mating success and female choice in a lek-breeding antelope

We investigated factors underlying variation in male matingsuccess in Uganda kob (Kobus kob thomasi), a lek-breeding antelope.We found that only heavy (and, possibly, relatively old) malesheld lek territories and that female choice was an importantdeterminant of nonrandom mating patterns at leks. Our measureof male mating success was closely related to the historicalpopularity of the territory that a male defended, and individualfemales showed consistent preferences for particular lek territories,despite changes in territory ownership. Male success increasedwith body weight and declined independently of territory effectsduring each bout of lek territory tenure. We also found someevidence that female kob copied one another's choice of matesbecause females arriving at a lek tended to join territoriesthat already had relatively large harems on them. When comparedacross leks, average male mating success increased with leksize. Our results suggest that female kob may use a suite ofmale- and territory-based cues in mate choice at leks and, asa result, mate with particularly large males. However, we wereunable to determine whether female kob gain any direct or indirectbenefits through mate choice at leks.     

Sexually selected sexual selection: Can evolutionary retribution explain female ornamental colour?

By preferring mates with increasingly costly ornaments or courtship displays, females cause an escalation of male reproductive costs. Such increased costs should promote male selectivity based on fecundity‐linked female attributes, leading to female ornamentation in species with traditional sex roles. Consequently, female ornamentation should evolve more frequently in taxa where male reproduction is costly than in comparable taxa where it is cheaper. We assessed the prevalence of female ornamental colouration in two clades of viviparous cyprinodontid fish: the Goodeinae, where stringent female choice imposes male mating costs, and the Poeciliinae, whose males can circumvent female mate choice. We found that although in the Poeciliinae female ornamental colour is a correlated, but paler version of male coloration, females of the Goodeinae often display vivid ornamental colours that are distinct from those of males. Thus, male and female ornaments are not (phylo)genetically correlated in the Goodeinae. Furthermore, phylogenetic signal on male and female colour is clearly detectable in the Poeciliinae, but absent in the Goodeinae, suggesting that ornamental colour of males and females in the latter may be the consequence of selection. Given that enforceable female choice has promoted male ornaments, we propose that evolutionary retribution has promoted distinct female ornaments in the Goodeinae.     

Within‐Species Mate Preferences Do Not Contribute to the Maintenance of Sexually Monomorphic Mating Signals in Green Lacewings

We know much less about the evolutionary forces and constraints that maintain similar mating displays in females and males than we do about sexually dimorphic mating displays. Both female and male green lacewings have sexually monomorphic vibrational mating signals and are equally choosy against heterospecific mating signals. This similarity in between‐species sex roles may explain a large part of the presence of species‐specific female signals in these species, but does not necessarily predict why female and male signals are similar. We tested for within‐species sex‐specific similarities in mate preferences in Chrysoperla lucasina that may contribute to the maintenance of sexually monomorphic mating signals in this species. We found weak preferences and low levels of discrimination for signals with varying fine‐scale temporal features (volley duration, period, and volley‐duty cycle). The longer signals that both sexes produced in response to playback were sexually monomorphic, but some females and most males also produced shorter signals with significantly reduced volley durations and periods. Notably, all of these signals had indistinguishable volley‐duty cycles, the ratio of volley duration to volley period. We propose that mating signals in C. lucasina are maintained in both sexes because of similar between‐species mate preferences, but the sexually monomorphic mating signals cannot be attributed to significant within‐species mate preferences. What differences are present in within‐species sex roles may be resolved by a male‐biased signal polymorphism, in long and short signals that are hypothesized to have distinct functions during mate calling and courtship.     

Maintenance of genetic variation in sexual ornaments: a review of the mechanisms

Female preferences for elaborate male sexual traits have been documented in a number of species in which males contribute only genes to the next generation. In such systems, mate choice has been hypothesised to benefit females genetically. For the genetic benefits to be possible there must be additive genetic variation (V(A)) for sexual ornaments, such that highly ornamented males can pass fitter genes on to the progeny of choosy females. Here, I review the mechanisms that can contribute to the maintenance of this variation. The variation may be limited to sexual ornaments, resulting in Fisherian benefits in terms of the increased reproductive success of male progeny produced by choosy females. Alternatively, ornaments may capture V(A) in other life-history traits. In the latter case, "good genes" benefits may apply in terms of improved performance of the progeny of either sex. Some mechanisms, however, such as negative pleiotropy, sexually antagonistic variation or overdominance, can maintain V(A )in ornaments and other life-history traits with little variation in total fitness, leaving little room for any genetic benefits of mate choice. Distinguishing between these mechanisms has consequences not only for the theory of sexual selection, but also for evolution of sex and for biological conservation. I discuss how the traditional ways of testing for genetic benefits can usefully be supplemented by tests detecting benefits resulting from specific mechanisms maintaining V(A )in sexual ornaments.     

Male versus female mate choice: sexual selection and the evolution of species recognition via reinforcement

Male mate choice, expressed through courtship preferences, sometime occurs even under the mating system of polygyny, when the operational sex ratio is skewed toward males. The conditions under which male mate choice may be expected during polygyny are not well established. Servedio and Lande (2006, Evolution 60:674-685), assuming strict polygyny where all females have equal mating success, show that when having a preference does not increase the amount of energy that a male can put into courtship, male preferences for "arbitrary" female ornaments should not be expected to evolve; direct selection acts against them because they place males that carry them into situations in which there is high competition for mates. Here I explore in detail two situations under which logic dictates that this effect may be overcome or reversed. First I determine the contributions that direct and indirect selection place on male versus female preferences for traits that increase viability, using notation that allows the exact expression of these measures of selection. I find that direct selection against male preferences still predominates in the male mate choice model, causing less evolution by male than female preferences under these conditions. Second I address whether male mate choice is likely to evolve as a mechanism of premating isolation leading to species recognition, driven by the process of reinforcement. Reinforcement is compared under male and female mate choice, using a variety of models analyzed by both analytical techniques assuming weak selection and numerical techniques under broader selective conditions. I demonstrate that although under many conditions stronger premating isolation evolves under female mate choice, reinforcement may indeed occur via male mate choice alone.     

The role of functional constraints in nonrandom mating patterns for a dance fly with female ornaments

Most hypotheses to explain nonrandom mating patterns invoke mate choice, particularly in species that display elaborate ornaments. However, conflicting selection pressures on traits can result in functional constraints that can also cause nonrandom mating patterns. We tested for functional load‐lifting constraints during aerial copulation in Rhamphomyia longicauda, a species of dance fly that displays multiple extravagant female‐specific ornaments that are unusual among sexual traits because they are under stabilizing selection. R. longicauda males provide females with a nuptial gift before engaging in aerial mating, and the male bears the entire weight of the female and nuptial gift for the duration of copulation. In theory, a male's ability to carry females and nuptial gifts could constrain pairing opportunities for the heaviest females, as reported for nonornamented dance flies. In concert with directional preferences for large females with mature eggs, such a load‐lifting constraint could produce the stabilizing selection on female size previously observed in this species. We therefore tested whether wild‐caught male R. longicauda collected during copulation were experiencing load‐lift limitations by comparing the mass carried by males during copulation with the male's wing loading traits. We also performed permutation tests to determine whether the loads carried by males during copulation were lighter than expected. We found that heavier males are more often found mating with heavier females suggesting that whereas R. longicauda males do not experience a load‐lift constraint, there is a strong relationship of assortative mating by mass. We suggest that active male mate choice for intermediately adorned females is more likely to be causing the nonrandom mating patterns observed in R. longicauda.     

Heterozygosity-based assortative mating in blue tits (Cyanistes caeruleus): implications for the evolution of mate choice

The general hypothesis of mate choice based on non-additive genetic traits suggests that individuals would gain important benefits by choosing genetically dissimilar mates (compatible mate hypothesis) and/or more heterozygous mates (heterozygous mate hypothesis). In this study, we test these hypotheses in a socially monogamous bird, the blue tit (Cyanistes caeruleus). We found no evidence for a relatedness-based mating pattern, but heterozygosity was positively correlated between social mates, suggesting that blue tits may base their mating preferences on partner''s heterozygosity. We found evidence that the observed heterozygosity-based assortative mating could be maintained by both direct and indirect benefits. Heterozygosity reflected individual quality in both sexes: egg production and quality increased with female heterozygosity while more heterozygous males showed higher feeding rates during the brood-rearing period. Further, estimated offspring heterozygosity correlated with both paternal and maternal heterozygosity, suggesting that mating with heterozygous individuals can increase offspring genetic quality. Finally, plumage crown coloration was associated with male heterozygosity, and this could explain unanimous mate preferences for highly heterozygous and more ornamented individuals. Overall, this study suggests that non-additive genetic traits may play an important role in the evolution of mating preferences and offers empirical support to the resolution of the lek paradox from the perspective of the heterozygous mate hypothesis.     

Male Mating History Influences Female Mate Choice in the Trinidadian Guppy (Poecilia reticulata)

Based on the phenotype‐linked fertility hypothesis, sexual selection should favour females that can accurately assess the recent mating history of available sexual partners and preferentially avoid mating with recently‐mated males [who may be sperm depleted (SD)] so as to minimize the risk of their eggs not being fertilized. This hypothesis has received to date only limited attention and empirical support. Therefore, in the current study, we investigated experimentally whether females of a vertebrate species, the Trinidadian guppy (Poecilia reticulata), are able to assess the recent mating history of males, and thus potentially their functional fertility, and choose to avoid mating with males that appear to have recently mated and who may be sperm limited. Individual virgin females were first given a dichotomous choice between a male that had not been recently observed to interact sexually with another female (i.e. not sperm‐depleted) and another male that had been observed to interact sexually with a female (i.e. potentially sperm‐depleted) as sexual partners. Paired males were matched for body length and coloration. Immediately following this test, the focal females were subjected to a free‐swimming mate‐choice test using the same paired stimulus males. As predicted, on average, female guppies avoided the apparently recently‐mated (and potentially sperm‐depleted) male and exhibited a significant preference for the other male not recently observed mating (and thus not likely sperm limited) during both tests. We do not yet fully understand the underlying mechanisms of this preference. Therefore, further research on the particular cues that females use to assess the recent mating history and fertility status of males is required.     

Males Benefit from Mating with Outbred Females in Drosophila littoralis: Male Choice for Female Genetic Quality?

The evolution and expression of mate choice behaviour in either sex depends on the sex‐specific combination of mating costs, benefits of choice and constraints on choice. If the benefits of choice are larger for one sex, we would expect that sex to be choosier, assuming that the mating costs and constraints on choice are equal between sexes. Because deliberate inbreeding is a powerful genetic method for experimental manipulation of the quality of study organisms, we tested the effects of both male and female inbreeding on egg and offspring production in Drosophila littoralis. Female inbreeding significantly reduced offspring production (mostly due to lower egg‐to‐adult viability), whereas male inbreeding did not affect offspring production (despite a slight effect of paternal inbreeding on egg‐to‐adult viability). As inbreeding depressed female quality more than male quality, the benefits of mate choice were larger for males than for females. In mate choice experiments, inbreeding did not affect male mating success (measured as a probability to be accepted as a mate in a large group), suggesting that females did not discriminate among inbred and outbred males. In contrast, female mating success was affected by inbreeding, with outbred females having higher mating success than inbred females. This result was not explained by lower activity of inbred females. Our results show that D. littoralis males benefit from mating with outbred females of high genetic quality and suggest adaptive male mate choice for female genetic quality in this species. Thus, patterns of mating success in mate choice trials mirrored the benefits of choice: the sex that benefited more from choice (i.e. males) was more choosy.     

Do Female Western Mosquitofish,Gambusia affinis,Prefer Ornaments That Males Lack?

Some species in the family Poeciliidae are known for extravagant male ornaments and courtship behavior (e.g., guppies), but the majority of poeciliids are characterized by coercive male copulation attempts that seem to circumvent female choice. In some lineages with male ornaments, female sensory bias may have preceded the evolution of corresponding male signals. We examined female preferences for colorful ornaments in Western mosquitofish, Gambusia affinis, in which males lack ornamentation and reproduce primarily through coercive mating attempts. We found that females exhibited a positional affinity for males that were artificially ornamented with blue coloration over males that had been treated with a transparent ornament. Females exhibited the opposite effect for males treated with red ornaments. In contrast, focal females did not exhibit behavioral discrimination between two live stimulus females or two models (silver fishing lures) with blue vs. transparent ornaments. This suggests a sexual context for female discrimination between males based on ornament color and whether an ornament was present. Because tribe Gambusiini is the basal branch of family Poeciliidae, the results of this study are consistent with the hypothesis that female responsiveness to male coloration is the ancestral poeciliid character state.     

Male sexual ornament size is positively associated with reproductive morphology and enhanced fertility in the stalk-eyed fly <Emphasis Type="Italic">Teleopsis dalmanni</Emphasis>

Background  

Exaggerated male ornaments and displays often evolve in species where males only provide females with ejaculates during reproduction. Although "good genes" arguments are typically invoked to explain this phenomenon, a simpler alternative is possible if variation in male reproductive quality (e.g. sperm number, ejaculate content, mating rate) is an important determinant of female reproductive success. The "phenotype-linked fertility hypothesis" states that female preference for male ornaments or displays has been selected to ensure higher levels of fertility and has driven the evolution of exaggerated male traits. Females of the stalk-eyed fly Teleopsis dalmanni must mate frequently to maintain high levels of fertility and prefer to mate with males exhibiting large eyespan, a condition-dependent sexual ornament. If eyespan indicates male reproductive quality, females could directly increase their reproductive success by mating with males with large eyespan. Here we investigate whether male eyespan indicates accessory gland and testis length, and then ask whether mating with large eyespan males affects female fertility.     

Context-dependent effects of tail-ornament damage on mating success in black grouse

Male black grouse (Tetrao tetrix) may receive damage to theirtail ornaments, the lyre, during goshawk predation attemptsand during fights with other males. In this study we confirma previous observation that black grouse males with damagedtail ornaments suffer reduced mating success. In males thatheld territories on the edge of the leks, tail damage was unrelatedto mating success, whereas in central males damage was negativelycorrelated with mating success. We tested experimentally whetherabsence of damage is used by females in mate choice. In maleswith edge territories, intact, control males had higher matingsuccess than males with cut tails, but in males with centralterritories, lyre cutting had no effect on mating success. Theseresults suggest two interpretations. First, female choice alsodepends on factors other than tail damage such as position onthe lek and dominance. Second, the effect of tail damage iscontext dependent; in males that otherwise meet females standards(e.g., dominant males), the effect of tail damage is negligible,but in less dominant males, tail damage could be used by femalesin mate selection. The second interpretation provides an explanationfor why the data on unmanipulated and manipulated birds differ.In experimental central birds, factors other than tail damageprobably determine male mating success, whereas in experimentaledge birds such factors are probably absent and therefore taildamage is relatively more important. In central unmanipulatedbirds, however, males with natural damage are probably not chosenbecause tail damage and absence of other attractive traits arecorrelated. The absence of an effect on peripheral unmanipulatedbirds may be explained by their overall low mating success     

Mate sampling and the sexual conflict over mating in seaweed flies

The order in which females encounter, or sample, males in apopulation may have important consequences for mate choice,with the information gathered about males influencing boththe preference function and degree of choosiness of females.Sexual selection may be affected as a result. Sampling of particularsubsets of males may be a crucial component of individual variation in mate preferences within populations. However, the sequencein which males are sampled may also be important in specieswithout traditional, active mate choice, such as when sexualselection involves sexual conflict over mating. This wouldoccur if the likelihood of a female mating with a male of acertain phenotype changes as a result of previous encounters.We examined the effects of encountering males differing inbody size, a sexually selected phenotype, in the seaweed flyCoelopa frigida. Sexual selection occurs in this species asa result of a sexual conflict over mating. We show that theoutcome of the sexual conflict is independent of the orderin which males are encountered by female seaweed flies, withthe overall mating advantage to large males being unaffected.In addition, we explored female preference functions and evaluatethe heterogeneity in female willingness to mate. We suggestthat consideration of mate sampling theory is valuable whenexamining mate choice in species in which sexual selectionis driven by sexual conflict.