Stickleback Males Increase Red Coloration and Courtship Behaviours in the Presence of a Competitive Rival

In species where females preferentially select the most colourful males, males may strategically invest in courtship and nuptial colour according to the presence of rivals. In this experimental study, we tested this in the three‐spined stickleback (Gasterosteus aculeatus) in which mature males exhibit carotenoid‐based red coloration to attract mates and defend their territories against male competitors. We challenged experimental males with either a red‐ornamented dummy male or a non‐ornamented dummy for five min per day in six‐d experimental trial, which was repeated twice during the breeding season. We found that the males presented with a coloured rival exhibited more frequent courtship behaviours (i.e. fanning and gluing) to females than those presented with a non‐coloured intruder during the second experimental trial. At the end of each trial, the experimental males also showed a significantly larger area of red coloration in the presence of a coloured intruder. Our findings suggest that male sticklebacks regulate mating effort according to the presence of competitive rivals by increasing their investment in costly signals when successful mating and territory defence is at risk.     

RESEARCH PAPER: Multiple Sexual Ornamentation Signals Male Quality and Predicts Female Preference in Minnows

Sexual ornamentation often consists of multiple components. Different sexual signals may indicate different aspects of mate quality or reflect quality in different time scales. On the other hand, same signals can have a dual function and are used both in male–male competition and courtship. Many fish species are capable of rapidly altering their colouration (ephemeral colour changes), but this capability is usually ignored in sexual selection studies. Here, we used experimentally manipulated social environments to study the ephemeral colour changes in multicomponent sexual signals of male minnows (Phoxinus phoxinus) during male–male competition and female choice. We found that the dominant males courted the females more actively and had redder and/or darker skin colouration than the subordinate males. Furthermore, darkness difference between subordinate and dominant males increased in the presence of female, which suggests that the male–male competition may increase the honesty of signalling and thus facilitate female choice. In support of this hypothesis, females had a strong behavioural preference towards the more colourful males, which may indicate female choice. As colourful males often had a higher social status than paler individuals, it is possible that females base their preference on male status, not only the colouration per se. In any case, our results suggest that sexual ornamentation of male minnows may signal status, courting activity and superior quality of the males and that these signals may have a dual function in both male–male competition and female choice. Females preferred different ornamental traits (dark and red colour patterns) relatively equally, indicating that mate choice is based on multiple cues.     

Ephemeral Sexual Dichromatism in Zebrafish (Danio rerio)

Secondary sexual displays may be overlooked in many species, especially when they are ephemerally expressed or imperceptible to human senses. Zebrafish (Danio rerio), like many schooling fish, do not appear sexually dichromatic, but previous anecdotal observations indicate that sexual colouration is expressed briefly during courtship (ephemeral nuptial colouration). Our goals were to compare colour estimates of male vs. female zebrafish using digital photography in situ, computer software and human observations. We found that both sexes changed their colour estimates during spawning (dark and light stripes) and that some sex differences (light stripes) were larger or only became apparent during this time. We also found that individual males that appeared more colourful and conspicuous to the human eye engaged in courtship more often than less conspicuous males. We detected differences in the colour estimates between wild‐derived vs. a laboratory strain of zebrafish and reduced individual variation in the laboratory strain. This is the first study to systematically and objectively quantify body colour in zebrafish by utilizing colour estimates, although further studies are needed to determine the underlying mechanisms and signalling functions of this sexual dichromatism.     

Experimental Addition of Green Plants to the Nest Increases Testosterone Levels in Female Spotless Starlings

Multiple male traits and displays may act in signalling sexually selected processes during courtship. Spotless starling males (Sturnus unicolor) carry green plants into their nests before egg laying, and recent studies have shown that this behaviour is related to female breeding decisions and the production of male‐biased broods. Although the functional implications of this effect on females are not yet clear, data suggest that it could be mediated by female circulating hormones. Additionally, females may show higher androgen levels as a consequence of the increased female–female competition generated by the increase in male attractiveness. We tested this hypothesis using the same manipulation of green nesting material that has been previously shown to result in an increase of male attractiveness in male spotless starlings. We found that females in experimental nests increased their circulating testosterone levels during the laying period. In addition, there was an increase of social interferences in the experimental nests because of the addition of green plants. We hypothesise that testosterone may allow females to maintain their mating status when competing with other females for the preferred males. Addition of green plants also increased the variance in the levels of circulating testosterone, suggesting plasticity between females in their response to the manipulation. We propose that there is a functional link between high testosterone levels, male‐biased sex ratios and female resource‐holding potential in intra‐sexual competition in this species.     

Reproductive Signals of Female Lizards: Pattern of Trait Expression and Male Response

Relative to the volume of studies concerning the function and evolution of male‐biased sexually dimorphic traits, instances of female‐biased sexual dimorphisms remain largely unstudied, especially in species with conventional sex roles. I investigated the signal function of a female‐specific ornamental trait using the striped plateau lizard (Sceloporus virgatus, Phrynosomatidae) as a model system. During the reproductive season, female S. virgatus develop orange color on their throats that is absent in conspecific males. I established the relationship between color expression and female reproductive state, and determined male response to female color. I show that dynamic changes occurring within the color patch can potentially identify each stage of the female reproductive cycle, largely because of a lag in patch growth relative to color intensification. Sexual receptivity is associated with intense patches rapidly growing in size; ovulation occurs near peak color expression; and the unreceptive period is associated with large patches fading in intensity. Because females express orange color during both the receptive and unreceptive periods, the pattern of color expression is consistent with the courtship‐stimulation and courtship‐rejection hypotheses of signal function. Males may preferentially associate with females that have more highly developed color patches during the courtship season, and/or ignore such females when they are unreceptive. An examination of male behavior towards unfamiliar females indicates that female color has a role in courtship stimulation but has little, if any, role in courtship rejection. During the pre‐mating season, males maintained significantly closer affiliation with, and tended to perform more social behavior towards females with more intense color. During the post‐mating season, female color had no apparent effect on male behavior. The evolution and current function of female ornaments may vary among taxonomically‐related species as a result of differences in ecology, social system, and life‐history.     

Regulation of eye and jaw colouration in three‐spined stickleback Gasterosteus aculeatus

Fish can change their skin and eye colour for background matching and signalling. Males of Gasterosteus aculeatus develop ornamental blue eyes and a red jaw during the reproductive season, colours that are further enhanced during courtship. Here, the effects of different hormones on physiological colour changes in the eyes and jaws of male and female G. aculeatus were investigated in vitro. In an in vivo experiment, G. aculeatus were injected with a receptor blocker of a pivotal hormone (noradrenaline) that controls colour change. In males, noradrenaline had aggregating effects on melanophore and erythrophore pigments resulting in blue eyes and a pale jaw, whereas melanocyte‐concentrating hormone (MCH) and melatonin resulted in a pale jaw only. When noradrenalin was combined with melanocyte stimulating hormone (MSH) or prolactin, the jaw became red, while the eyes remained blue. In vivo injection of yohimbine, an alpha‐2 adrenoreceptor blocker, resulted in dispersion of melanophore pigment in the eyes and inhibited the blue colouration. Altogether, the data suggest that noradrenalin has a pivotal role in the short‐term enhancement of the ornamental colouration of male G. aculeatus, potentially together with MSH or prolactin. This study also found a sex difference in the response to MCH, prolactin and melatonin, which may result from different appearance strategies in males, versus the more cryptic females.     

Sperm competition generates evolution of increased paternal investment in a sex role‐reversed seed beetle

When males provide females with resources at mating, they can become the limiting sex in reproduction, in extreme cases leading to the reversal of typical courtship roles. The evolution of male provisioning is thought to be driven by male reproductive competition and selection for female fecundity enhancement. We used experimental evolution under male‐ or female‐biased sex ratios and limited or unlimited food regimes to investigate the relative roles of these routes to male provisioning in a sex role‐reversed beetle, Megabruchidius tonkineus, where males provide females with nutritious ejaculates. Males evolving under male‐biased sex ratios transferred larger ejaculates than did males from female‐biased populations, demonstrating a sizeable role for reproductive competition in the evolution of male provisioning. Although larger ejaculates elevated female lifetime offspring production, we found little evidence of selection for larger ejaculates via fecundity enhancement: males evolving under resource‐limited and unlimited conditions did not differ in mean ejaculate size. Resource limitation did, however, affect the evolution of conditional ejaculate allocation. Our results suggest that the resource provisioning that underpins sex role reversal in this system is the result of male–male reproductive competition rather than of direct selection for males to enhance female fecundity.     

Social context influences aggressive and courtship behavior in a cichlid fish

Social interactions require knowledge of the environment and status of others, which can be acquired indirectly by observing the behavior of others. When being observed, animals can also alter their signals based on who is watching. Here we observed how male cichlid fish (Astatotilapia burtoni) behave when being watched in two different contexts. In the first, we show that aggressive and courtship behaviors displayed by subordinate males depends critically on whether dominant males can see them, and in the second, we manipulated who was watching aggressive interactions and showed that dominant males will change their behavior depending on audience composition. In both cases, when a more dominant individual is out of view and the audience consists of more subordinate individuals, those males signal key social information to females by displaying courtship and dominant behaviors. In contrast, when a dominant male is present, males cease both aggression and courtship. These data suggest that males are keenly aware of their social environment and modulate their aggressive and courtship behaviors strategically for reproductive and social advantage.     

It Takes Two to Tango: Relative Influence of Male and Female Identity and Morphology on Complex Courtship Display in a Newt Species

Consistency in behaviour is currently receiving a renewed interest. Although courtship display is generally consistent in terms of behavioural sequence and structure, there is also commonly important variation in the intensity of courtship display between and within males of a given species. Indeed, not all males have the same ability to perform courtship display (variation between males), and each male can potentially adjust his courtship effort in response to the environment (variation within a male). Although the study of male courtship display has received considerable attention in recent years, it is still unclear which part of the variation can be explained by male ability or motivation. We investigated this issue on two phases of the complex courtship display of the palmate newt Lissotriton helveticus. Overall, we found that both male and female identities affected courtship behaviour, but the relative influence of each sex depended on the courtship phase. Male identity explained variation in fan and creep‐quiver display, whereas female identity explained variation in creep‐quiver only. Interestingly, we did not find any link between the expression of courtship display and male or female morphological traits. Our study showed consistency of male courtship display in newts and successfully dissects the different sources of variation that can affect behavioural repeatability/consistency of courtship display.     

Genetic evidence for male‐biased dispersal in the Qinghai toad‐headed agamid Phrynocephalus vlangalii and its potential link to individual social interactions

Sex‐biased dispersal has profound impacts on a species' biology and several factors have been attributed to its evolution, including mating system, inbreeding avoidance, and social complexity. Sex‐biased dispersal and its potential link to individual social interactions were examined in the Qinghai toad‐headed agamid (Phrynocephalus vlangalii). We first determined the pattern of sex‐biased dispersal using population genetic methods. A total of 345 specimens from 32 sites in the Qaidam Basin were collected and genotyped for nine microsatellite DNA loci. Both individual‐based assignment tests and allele frequency‐based analyses were conducted. Females revealed much more genetic structure than males and all results were consistent with male‐biased dispersal. First‐generation migrants were also identified by genetic data. We then examined eight social interaction‐related morphological traits and explored their potential link to sex‐biased dispersal. Female residents had larger heads and longer tails than female migrants. The well‐developed signal system among females, coupled with viviparity, might make remaining on natal sites beneficial, and hence promote female philopatry. Dominant females with larger heads were more likely to stay. Contrary to females, male migrants had larger heads and belly patches than residents, suggesting that dispersal might confer selective advantages for males. Such advantages may include opportunities for multiple mating and escaping from crowded sites. Large belly patches and several other morphological traits may assist their success in obtaining mates during dispersal. Furthermore, a relatively high relatedness (R = 0.06) among females suggested that this species might have rudimentary social structure. Case studies in “less” social species may provide important evidence for a better understanding of sex‐biased dispersal.     

Flexible mate choice when mates are rare and time is short

Female mate choice is much more dynamic than we once thought. Mating decisions depend on both intrinsic and extrinsic factors, and these two may interact with one another. In this study, we investigate how responses to the social mating environment (extrinsic) change as individuals age (intrinsic). We first conducted a field survey to examine the extent of natural variation in mate availability in a population of threespine sticklebacks. We then manipulated the sex ratio in the laboratory to determine the impact of variation in mate availability on sexual signaling, competition, and mating decisions that are made throughout life. Field surveys revealed within season heterogeneity in mate availability across breeding sites, providing evidence for the variation necessary for the evolution of plastic preferences. In our laboratory study, males from both female‐biased and male‐biased treatments invested most in sexual signaling late in life, although they competed most early in life. Females became more responsive to courtship over time, and those experiencing female‐biased, but not male‐biased sex ratios, relaxed their mating decisions late in life. Our results suggest that social experience and age interact to affect sexual signaling and female mating decisions. Flexible behavior could mediate the potentially negative effects of environmental change on population viability, allowing reproductive success even when preferred mates are rare.     

Social effects on fruit fly courtship song

Courtship behavior in Drosophila has often been described as a classic innate behavioral repertoire, but more recently extensive plasticity has been described. In particular, prior exposure to acoustic signals of con‐ or heterspecific males can change courtship traits in both sexes that are liable to be important in reproductive isolation. However, it is unknown whether male courtship song itself is socially plastic. We examined courtship song plasticity of two species in the Drosophila melanogaster subgroup. Sexual isolation between the species is influenced by two male song traits, the interpulse interval (IPI) and sinesong frequency (SSF). Neither of these showed plasticity when males had prior experience of con‐ and heterospecific social partners. However, males of both species produced longer bursts of song during courtship when they were exposed to social partners (either con‐ or heterospecific) than when they were reared in isolation. D. melanogaster carrying mutations affecting short‐ or medium‐term memory showed a similar response to the social environment, not supporting a role for learning. Our results demonstrate that the amount of song a male produces during courtship is plastic depending on the social environment, which might reflect the advantage of being able to respond to variation in intrasexual competition, but that song structure itself is relatively inflexible, perhaps due to strong selection against hybridization.     

The Association Between Personality Traits,Morphological Traits and Alternative Mating Behaviour in Male Endler's Guppies,Poecilia wingei

Alternative mating behaviour, personality traits and morphological characters are predicted to be correlated. Bolder, larger and more colourful males are expected to preferentially court females, while shy, small and drab‐coloured individuals are predicted to sneak copulations. We used males of Endler's guppy, Poecilia wingei, to test this association over a long temporal period (hence including ontogenetic changes) and under two social environments (male‐biased and female‐biased). We found that personality traits (exploration, boldness, activity) of P. wingei males were highly repeatable across long time spans, but they were not correlated (formed no behavioural syndrome). Male age and social environment had no effect on any personality trait, despite their effects on alternative mating behaviour. Young males with higher activity levels were more likely to attempt sneaking. In older fish, there was an association between orange coloration, courtship and boldness, but this was not observed in young males. Our results suggest that alternative mating behaviour is more flexible than personality traits and is independent of them. Non‐colour‐based morphological traits (gonopodium length, body length, caudal straps length, dorsal fin length) were not correlated with any particular mating behaviour.     

Complex Courtship Behavior in the Striped Ground Cricket, Allonemobius socius (Orthoptera: Gryllidae): Does Social Environment Affect Male and Female Behavior?

Complex courtship in the striped ground cricket, Allonemobius socius, involves a series of behaviors alternating between the sexes. We examined if complex courtship allows either or both genders to evaluate their mate and how mating behavior changes in different social environments. While complex courtship may allow discrimination by both sexes, here only females exhibited a preference. Males did not alter their courtship behavior or change spermatophore size for different size females. In contrast, females initiated copulation more quickly with bigger males possessing bigger spermatophores. In a different social environment (additional male, female, or both), males were less likely to omit courtship songs and female discrimination of mates changed. The distinct differences in male and female behavior suggest that subtle changes in social environment can have important consequences in structuring courtship and mating behavior.     

A Young Manakin Knows His Place: Evidence for an Age‐Graded Dominance Hierarchy Among Long‐Tailed Manakins

In lek‐breeding systems where many males gather at display sites, males benefit from the establishment of dominance hierarchies to reduce intrasexual aggression and the associated risk of injuries. Long‐tailed manakins (Chiroxiphia linearis) exhibit an exploded lek‐breeding system wherein the two top‐ranking males at each display site team up to perform elaborate coordinated courtship displays for females. Young males undergo delayed plumage maturation whereby they acquire distinct pre‐definitive plumage patterns each year until they attain definitive plumage in their fifth year. This unique characteristic is thought to have evolved as a status‐signalling mechanism to aid in the establishment of an age‐graded dominance hierarchy in which older males are dominant to younger males. Previous research has shown evidence for such a dominance hierarchy among alpha and beta males; however, the presence of this hierarchy among males of other age classes has never been quantified. In this study, we investigated the presence of an age‐graded dominance hierarchy by determining whether older males direct more aggressive behaviours towards younger males. We also investigated whether status signalling is less clear within age classes than between age classes, by determining whether males within the same age class exhibit more aggression towards each other. We found that older males performed aggressive behaviours towards younger males much more frequently than younger males performed aggressive behaviours towards older males. We also found that some aggressive interactions occurred between males within the same age class more frequently than between males from different age classes. Our study provides some evidence for an age‐graded dominance hierarchy among male long‐tailed manakins of all age classes and also provides some support for the status‐signalling hypothesis. However, further research is needed to conclusively establish the presence of a linear dominance hierarchy among younger male manakins. This research may help us better understand the evolution of complex hierarchical systems in animals.     

It's not just what you have,but how you use it: solar‐positional and behavioural effects on hummingbird colour appearance during courtship

Animals exhibit a diversity of colours that can play key roles in mating interactions. However, we presently lack an understanding of the relative importance of the environment, behaviour and natural reflective properties of colourful ornaments in shaping an individual's colour appearance during mating displays. We investigated interactions among structurally based plumage, display environments and courtship shuttle displays of male Costa's hummingbirds (Calypte costae) to test how these elements may differentially contribute to colour appearance during shuttles. Male position relative to the sun was the strongest predictor of colour appearance, with shuttle behaviours and feather reflectance playing smaller roles. Furthermore, male solar orientation and shuttling behaviour (e.g. shuttle width) were repeatable among displays, whereas male colour appearance mostly was not. These results emphasise the contributions of behaviour and environment to colour‐signalling and suggest that relying on reflectance measurements of colourful ornaments alone provides an incomplete picture of ecologically relevant visual phenotypes of displaying animals.     

Cross‐fostering eggs reveals that female collared flycatchers adjust clutch sex ratios according to parental ability to invest in offspring

Across animal taxa, reproductive success is generally more variable and more strongly dependent upon body condition for males than for females; in such cases, parents able to produce offspring in above‐average condition are predicted to produce sons, whereas parents unable to produce offspring in good condition should produce daughters. We tested this hypothesis in the collared flycatcher (Ficedula albicollis) by cross‐fostering eggs among nests and using the condition of foster young that parents raised to fledging as a functional measure of their ability to produce fit offspring. As predicted, females raising heavier‐than‐average foster fledglings with their social mate initially produced male‐biased primary sex ratios, whereas those raising lighter‐than‐average foster fledglings produced female‐biased primary sex ratios. Females also produced male‐biased clutches when mated to males with large secondary sexual characters (wing patches), and tended to produce male‐biased clutches earlier within breeding seasons relative to females breeding later. However, females did not adjust the sex of individuals within their clutches; sex was distributed randomly with respect to egg size, laying order and paternity. Future research investigating the proximate mechanisms linking ecological contexts and the quality of offspring parents are able to produce with primary sex‐ratio variation could provide fundamental insight into the evolution of context‐dependent sex‐ratio adjustment.     

Density‐dependent sex‐biased development of macroptery in a water strider

In wing‐polymorphic insects, wing morphs differ not only in dispersal capability but also in life history traits because of trade‐offs between flight capability and reproduction. When the fitness benefits and costs of producing wings differ between males and females, sex‐specific trade‐offs can result in sex differences in the frequency of long‐winged individuals. Furthermore, the social environment during development affects sex differences in wing development, but few empirical tests of this phenomenon have been performed to date. Here, I used the wing‐dimorphic water strider Tenagogerris euphrosyne to test how rearing density and sex ratio affect the sex‐specific development of long‐winged dispersing morphs (i.e., sex‐specific macroptery). I also used a full‐sib, split‐family breeding design to assess genetic effects on density‐dependent, sex‐specific macroptery. I reared water strider nymphs at either high or low densities and measured their wing development. I found that long‐winged morphs developed more frequently in males than in females when individuals were reared in a high‐density environment. However, the frequency of long‐winged morphs was not biased according to sex when individuals were reared in a low‐density environment. In addition, full‐sib males and females showed similar macroptery incidence rates at low nymphal density, whereas the macroptery incidence rates differed between full‐sib males and females at high nymphal density. Thus complex gene‐by‐environment‐by‐sex interactions may explain the density‐specific levels of sex bias in macroptery, although this interpretation should be treated with some caution. Overall, my study provides empirical evidence for density‐specific, sex‐biased wing development. My findings suggest that social factors as well as abiotic factors can be important in determining sex‐biased wing development in insects.